Article

Volatile communication between plants that affects herbivory: A meta-analysis

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  • University of Hawaii
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Abstract

Volatile communication between plants causing enhanced defence has been controversial. Early studies were not replicated, and influential reviews questioned the validity of the phenomenon. We collected 48 well-replicated studies and found overall support for the hypothesis that resistance increased for individuals with damaged neighbours. Laboratory or greenhouse studies and those conducted on agricultural crops showed stronger induced resistance than field studies on undomesticated species, presumably because other variation had been reduced. A cumulative analysis revealed that early, non-replicated studies were more variable and showed less evidence for communication. Effects of habitat and plant growth form were undetectable. In most cases, the mechanisms of resistance and alternative hypotheses were not considered. There was no indication that some response variables were more likely to produce large effects. These results indicate that plants of diverse taxonomic affinities and ecological conditions become more resistant to herbivores when exposed to volatiles from damaged neighbours.

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... Plants under herbivore attack alter their volatile profile which can subsequently become attractive to natural enemies, so-called "cries for help" (Turlings et al. 1990). These signals can be also used for the upregulation of defence in other plants (Heil 2014;Karban et al. 2014;Ninkovic et al. 2021). This idea of plant-plant communication has transitioned from scepticism (Fowler and Lawton 1985) via tentative acceptance (Dicke and Bruin 2001) to widespread acceptance (Dicke et al. 2003;Heil and Karban 2010;Ninkovic et al. 2021). ...
... This idea of plant-plant communication has transitioned from scepticism (Fowler and Lawton 1985) via tentative acceptance (Dicke and Bruin 2001) to widespread acceptance (Dicke et al. 2003;Heil and Karban 2010;Ninkovic et al. 2021). Plants can communicate through the air (Farmer and Ryan 1990;Karban et al. 2014) and below-ground root and mycorrhizal networks (van Dam and Bouwmeester 2016). ...
... activated when needed; reviewed by Orians 2005;Ninkovic et al. 2021). The induced VOCs can deter herbivores (De Moraes et al. 2001), attract their predators and parasitoids (Kessler and Baldwin 2001;, convey information relating to herbivore attack to other parts of the same plant (Frost et al. 2007;Li and Blande 2017), and prime neighbouring plants against herbivore attack (Karban et al. 2014). Distress signals from a neighbouring plant can prime recipient plants to upregulate their defences in preparation for future attacks (Hilker and Schmülling 2019). ...
Article
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Trees can emit volatile organic compounds (VOCs) when under attack by herbivores, and these signals can also be detected by natural enemies and neighbouring trees. There is still limited knowledge of intra- and inter-specific communication in diverse habitats. We studied the effects of induced VOC emissions by three Ficus species on predation on the focal Ficus trees in a lowland tropical rainforest in Papua New Guinea. Further we assessed predation across a phylogenetically diverse set of neighbouring tree species. Two of the focal tree species, Ficus pachyrrhachis and F. hispidioides, have strong alkaloid-based constitutive defences while the third one, F. wassa, is lower in constitutive chemical defences. We experimentally manipulated the jasmonic acid signalling pathway by spraying the focal individuals with either methyl jasmonate (MeJA) or diethyldithiocarbamic acid (DIECA). These treatments induce increases or decreases in VOC emissions, respectively. We tested the possible effects of VOC emissions on each focal Ficus tree and two of its neighbours by measuring the predation rate of plasticine caterpillars. We found that predation increased after the MeJA application in only one focal tree species, F. wassa, while the DIECA application had no effect on any of the three focal species. Further, we did not detect an effect of our treatments on predation rates across neighbouring trees. Neither the phylogenetic distance of the neighbouring tree from the focal tree nor the physical distance from the focal tree had any effect on predation rates for any of the three focal Ficus species. These results suggest that even congeneric tree species vary in their response to the MeJA and DIECA treatment and subsequent response to VOC emissions by predators. Our results also suggest that MeJA effects did not spill over to neighbouring trees in highly diverse tropical rainforest vegetation.
... Plastic changes that are induced by plant-to-plant communication could affect roots through byproducts of physiological mechanisms. Plant-to-plant communications often lead to increases in the content of secondary chemical metabolites in leaves [7][8][9][10][11][12][13][14][15][16] or changes in shoot-to-root allocation 17 . The increase in secondary chemical metabolites may affect the microbial community associated with roots because secondary chemical metabolites have anti-microbial properties [18][19][20][21] . ...
... Similar to many previous studies 6,7,11 , our experiment demonstrated that the plant-to-plant communication induced changes in plant quality. Although plant biomass, shoot-to-root ratio and total phenolics in leaves were not affected (Fig. 1a-c), the saponins in both leaves and roots were significantly higher in the VOC-exposed plants (Fig. 1e,f). ...
... Our results are consistent with those of Shiojiri et al. 11 who showed that the VOCs from cut goldenrod increase the defense of soybean plants against the herbivore, S. litura. The response of soybean plants may reduce leaf damage through resistance effects [6][7][8] or alteration of herbivore behavior 9 . ...
Article
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Aboveground communication between plants is well known to change defense traits in leaves, but its effects on belowground plant traits and soil characteristics have not been elucidated. We hypothesized that aboveground plant-to-plant communication reduces root nodule symbiosis via induction of bactericidal chemical defense substances and changes the soil nutrient environment. Soybean plants were exposed to the volatile organic compounds (VOCs) from damaged shoots of Solidago canadensi s var. scabra , and leaf defense traits (total phenolics, saponins), root saponins, and root nodule symbiosis traits (number and biomass of root nodules) were measured. Soil C/N ratios and mineral concentrations were also measured to estimate the effects of resource uptake by the plants. We found that total phenolics were not affected. However, plants that received VOCs had higher saponin concentrations in both leaves and roots, and fewer root nodules than untreated plants. Although the concentrations of soil minerals did not differ between treatments, soil C/N ratio was significantly higher in the soil of communicated plants. Thus, the aboveground plant-to-plant communication led to reductions in root nodule symbiosis and soil nutrient concentrations. Our results suggest that there are broader effects of induced chemical defenses in aboveground plant organs upon belowground microbial interactions and soil nutrients, and emphasize that plant response based on plant-to-plant communications are a bridge between above- and below-ground ecosystems.
... Apart from influencing atmospheric chemistry and climate feedback, biogenic VOCs have multiple ecological functions, for example attracting and/or repelling herbivorous insects, recruiting natural enemies of the attacking herbivores, and mediating between-and within-plant communication, among others (De Moraes et al., 1998;Karban et al., 2014;Li and Blande, 2017;Tooker and Hanks, 2006). Moreover, some plant VOCs, such as isoprene and monoterpenes, have been shown to confer plants with thermal protection against high temperature-induced oxidative stress Loreto and Fineschi, 2015). ...
... The lack of a clear effect of gall-infestation on isoprene emissions observed in our study might be due to VOC-mediated withinand between-plant signalling. VOCs emitted from herbivoredamaged plants have been well documented to induce and/or prime VOC emissions from undamaged tissues of the same damaged plants as well as from neighbouring undamaged plants (Karban et al., 2014;Li and Blande, 2017). In hybrid aspen, for instance, herbivoreinduced VOCs were observed to enhance isoprene emissions from undamaged branches of the damaged saplings (Li and Blande, 2017). ...
... In hybrid aspen, for instance, herbivoreinduced VOCs were observed to enhance isoprene emissions from undamaged branches of the damaged saplings (Li and Blande, 2017). The galled and ungalled branches in our experimental plots were spaced 20-70 cm apart, which falls within the distance over which VOCmediated within-and between-plant signalling can occur in nature (Karban et al., 2014), and further, the branches might be connected to each other below ground. Therefore, it is possible that gall-infested branches might have stimulated isoprene emissions from neighbouring uninfested branches via both vascular and airborne signals, which in turn may have overshadowed the direct effects of gall infestation on isoprene emissions. ...
Article
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Climate change is altering high-latitude ecosystems in multiple facets, including increased insect herbivory pressure and enhanced emissions of volatile organic compounds (VOCs) from vegetation. Yet, joint impacts of climatic drivers and insect herbivory on VOC emissions from the Arctic remain largely unknown. We examined how one-month warming by open-top plastic tents, yielding a 3–4 °C air temperature increase, and the natural presence of gall-forming eriophyoid mites, Aculus tetanothrix, individually and in combination, affect VOC emissions from whortle leaved willow, Salix myrsinites, at two elevations in an Arctic heath tundra of Abisko, Northern Sweden. We measured VOC emissions three times in the peak growing season (July) from intact and gall-infested branches using an enclosure technique and gas chromatography–mass spectrometry, and leaf chemical composition using near-infrared reflectance spectroscopy (NIRS). Isoprene accounted for 91% of the VOCs emitted by S. myrsinites. Isoprene emission rates tended to be higher at the high than low elevation during the measurement periods (42 μg g⁻¹ DW h⁻¹ vs. 23 μg g⁻¹ DW h⁻¹) even when temperature differences were accounted for. Experimental warming increased isoprene emissions by approximately 54%, but decreased emissions of some minor compound groups, such as green leaf volatiles (GLVs) and (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT). In contrast, gall-infestation did not affect isoprene emissions but stimulated emissions of DMNT, sesquiterpenes and GLVs, particularly under ambient conditions at the low elevation. The NIRS-based chemical composition of the leaves varied between the two elevations and was affected by warming and gall-infestation. Our study suggests that under elevated temperatures, S. myrsinites increases emissions of isoprene, a highly effective compound for protection against oxidative stress, while an infestation by A. tetanothrix mites induces emissions of herbivore enemy attractants like DMNT, sesquiterpenes and GLVs. Under both conditions, warming effects on isoprene remain but mite effects on DMNT, sesquiterpenes and GLVs diminish.
... The compositions of HIPV blends are typically specific to the identity of the plant and the attacking herbivore species, conveying detailed information to other members of the ecological community, including natural enemies (Clavijo McCormick et al. 2012), other herbivores (Ray et al. 2020), and even other plants (Arimura et al. 2009). A growing number of studies have reported that plants can detect HIPVs from herbivore-damaged neighbors as a warning of possible herbivory and respond by enhancing their defenses (Karban et al. 2014). Here, we examine the specificity of plant responses to HIPVs by exposing plants to species-specific HIPV blends induced by three different herbivore attackers and quantifying plant defense activation. ...
... A surprising finding from our study was that exposure to saltmarsh caterpillar-induced HIPVs suppressed defense responses in neighboring plants (Fig. 3A-B), enhancing their susceptibility to caterpillar herbivory ( Fig. 2A). The majority of studies on plant responses to HIPVs have reported increased resistance to herbivory, highlighting interplant communication as a potential strategy for plants to better predict and defend against herbivore attack (Karban et al. 2014). In contrast, HIPV-mediated defense suppression has only been reported for a few plant-herbivore species combinations (Pearse et al. 2012;Li and Blande 2015;Zhang et al. 2019), and, more recently, plant exposure to an insect pheromone was also shown to suppress defenses (Brosset et al. 2021). ...
Article
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In response to herbivory, plants emit volatile compounds that play important roles in plant defense. Herbivore-induced plant volatiles (HIPVs) can deter herbivores, recruit natural enemies, and warn other plants of possible herbivore attack. Following HIPV detection, neighboring plants often respond by enhancing their anti-herbivore defenses, but a recent study found that herbivores can manipulate HIPV-interplant communication for their own benefit and suppress defenses in neighboring plants. Herbivores induce species-specific blends of HIPVs and how these different blends affect the specificity of plant defense responses remains unclear. Here we assessed how HIPVs from zucchini plants ( Cucurbita pepo ) challenged with different herbivore species affect resistance in neighboring plants. Volatile “emitter” plants were damaged by one of three herbivore species: saltmarsh caterpillars ( Estigmene acrea ), squash bugs ( Anasa tristis ), or striped cucumber beetles ( Acalymma vittatum ), or were left as undamaged controls. Neighboring “receiver” plants were exposed to HIPVs or control volatiles and then challenged by the associated herbivore species. As measures of plant resistance, we quantified herbivore feeding damage and defense-related phytohormones in receivers. We found that the three herbivore species induced different HIPV blends from squash plants. HIPVs induced by saltmarsh caterpillars suppressed defenses in receivers, leading to greater herbivory and lower defense induction compared to controls. In contrast, HIPVs induced by cucumber beetles and squash bugs did not affect plant resistance to subsequent herbivory in receivers. Our study shows that herbivore species identity affects volatile-mediated interplant communication in zucchini, revealing a new example of herbivore defense suppression through volatile cues.
... Evidence has accumulated that plants can also eavesdrop on volatile cues emitted from neighbouring plants, and prime their defences in response, rendering those eavesdroppers more resistant to herbivorous insects (Frost et al. 2008;Karban et al. 2014a). The message sent by these cues is often interpreted as an 'alert' of a risk of herbivory for receiver-plants, which may enter into a state of readiness that enables the induction of earlier or stronger defences in response to subsequent attack (Pastor et al. 2013;Hilker et al. 2016). ...
... In the same year, Rhoades (1983) showed that Salix sitchensis trees growing near to caterpillar-infested neighbours had increased resistance to herbivores. Although these studies have received criticism, since then there has been an accumulation of evidence that plants can respond to VOCs emitted by their neighbours (Karban et al. 2014a). To date, more than 150 papers have been published on the subject with the main goal being to determine how exposure to VOCs enhances the defence and resistance to herbivores of receiver plants (non-filtered search for "plant-plant interaction" and "plant volatile" in ISI Web of Science the 24/02/2022). ...
Thesis
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The file displays only the currently published work. Upcoming publications do not appear in the PDF. This thesis explores whether the process of domestication may have affected plant VOC responses to (i) feeding from a specialist herbivore; (ii) elevated ozone; (iii) both stresses sequentially. It also examines whether volatile-mediated plant to plant interactions are more effective in wild than cultivated varieties and evaluates whether HIPVs affect photosynthesis rate, stomatal conductance, growth and reproduction of receiver plants. In nature, it is not only plants that release VOCs, but herbivorous insects also rely on VOC emissions for their survival. Therefore, to further explore plant responses to different biotic stimuli, the thesis ends by investigating whether plants eavesdrop on insect-derived VOCs and prime their defences in response. This thesis was accomplished through four years of research on different wild and cultivated Brassicaeous plants and their antagonistic specialist insect herbivore Plutella xylostella.
... The indirect defense is mainly achieved by attracting beneficial insects (such as predators) from additional trophic levels [6]. Being the most common attractant to these predators, volatile organic compounds (VOCs) secreted by plants are mainly terpenes, fatty acid derivatives, and some other aromatic compounds [7][8][9], they can not only function in the defense process of a single individual, but some can also act as "alarms" to inform other plants to start defense [10][11][12]. ...
... Plants can communicate via volatile chemicals. Studies have shown that when plants are injured, adjacent plants initiate the corresponding mechanism of chemical defense [10][11][12]. In this study, β-myrcene and linalool were found in healthy H. punctata individuals near wounded individuals. ...
Article
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Plants have evolved various self-defense mechanisms against insect feeding. There are many reports regarding both direct and indirect defense mechanisms in seed-plant. However, only direct defenses on ferns were considered and the indirect defense mechanism has never been reported. In this study, it was observed that the fern Hypolepis punctata can attract the assassin bug Sclomina erinacea in the field. We collected and analyzed volatiles from H. punctata healthy individuals and the ones wounded by Bertula hadenalis, using dynamic headspace and GC-MS. We recorded the electroantennogram responses of antennae of S. erinacea to different standards of volatile compounds identified from the GC-MS analysis. We also analyzed the behavior of male and female S. erinacea adults in response to volatiles collected from H. punctata using a Y-tube olfactometer. The results showed that a number of volatile compounds were produced when the fern was damaged by B. hadenalis. Electroantennography and Y-tube olfactometer results showed that some herbivore-induced volatiles and volatiles from undamaged leaves could attract S. erinacea. Our research suggests that H. punctata can attract insect predators by releasing herbivory-induced volatile organic compounds, and for the first time we found ferns may also have indirect defense mechanisms using volatile organic compounds.
... Plants emit volatile organic compounds (VOCs) in response to leaf damage caused by herbivorous arthropods or mechanical damage such as weeding (Takabayashi & Shiojiri, 2019). When neighboring plants receive such VOCs, they often induce defenses against herbivores; this phenomenon is referred to as plant-plant communication (Heil & Bueno, 2007;Heil & Karban, 2010;Karban et al., 2000Karban et al., , 2014Shiojiri & Karban, 2008b;Tscharntke et al., 2001;Yoneya & Takabayashi, 2014). For example, field-grown sagebrush trees (Artemisia tridentata) which were exposed to VOCs from clipped conspecific plants in the early season experienced less herbivore damage in the following seasons (Shiojiri & Karban, 2008a). ...
... Lima bean (Phaseolus lunatus) plants exposed to VOCs from herbivore-damaged conspecific plants increased the amount of extrafloral nectar that attracts carnivorous arthropods (Choh et al., ,2004Heil & Kost, 2006). Plant-plant communication mediated by VOCs has been observed in >40 plant species, most of which are herbaceous (Heil & Karban, 2010;Karban et al., 2014;Li, 2016;Yoneya & Takabayashi, 2014). However, the first evidence of the phenomenon was found in tree species such as sugar maple and poplar (Baldwin & Schultz, 1983). ...
Article
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In response to volatiles emitted from a plant infested by herbivorous arthropods, neighboring undamaged conspecific plants become better defended against herbivores; this is referred to as plant‒plant communication. Although plant‒plant communication occurs in a wide range of plant species, most studies have focused on herbaceous plants. Here, we investigated plant‒plant communication in beech trees in two experimental plantations in 2018 and one plantation in 2019. Approximately 20% of the leaves of a beech tree were clipped in half in the spring seasons of 2018 and 2019 (clipped tree). The damage levels to leaves in the surrounding undamaged beech trees were evaluated 90 days after the clipping (assay trees). In both years, the damage levels decreased with a reduction in the distance from the clipped tree. In 2019, we also recorded the damage levels of trees that were not exposed to volatiles (nonexposed trees) as control trees and found that those that were located <5 m away from clipped trees had significantly less leaf damage than nonexposed trees. By using a gas chromatograph–mass spectrometer, ten and eight volatile compounds were detected in the headspaces of clipped and unclipped leaves, respectively. Among them, the amount of (Z)-3-hexenyl acetate in clipped leaves was significantly higher than that in nonclipped leaves. Our result suggests that green leaf volatiles such as (Z)-3-hexenol and (Z)-3-hexenyl acetate and other volatile organic compounds emitted from clipped trees induced defenses in the neighboring trees within the 5 m radius. The effective distances of plant‒plant communication in trees were discussed from the viewpoint of the arthropod community structure in forest ecosystems.
... The scientific discourse that ensued threw doubt on the conclusions (Fowler and Lawton, 1985) and temporarily slowed progress in the field (Karban et al., 2014a). However, a wealth of studies since has provided a solid literature base supporting the paradigm that plants release VOCs that can be detected by and elicit responses in their neighbours (Karban et al., 2014b). ...
... A common observation has been that exposure to herbivoreinduced plant volatiles (HIPVs) elicits changes in a receiver plant that decreases the cumulative seasonal herbivore damage to that receiver (Dolch and Tscharntke, 2000;Tscharntke et al., 2001;Karban and Maron, 2002;Karban et al., 2006). The frequency with which this observation has been reported provides compelling evidence that volatile-mediated plant-plant interactions are ecologically significant (Karban et al., 2014b), and great progress has been made in elucidating the integration of VOCs into plant defence mechanisms (Erb, 2019;Ye et al., 2019). These mechanisms encompass the detection of VOCs and the triggering of sophisticated molecular pathways , and the associational resistance facilitated through chemical camouflage (Himanen et al., 2010;Mofikoya et al., 2017;Bui et al., 2021). ...
Article
Full-text available
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 defence-related responses of receiver plants. However, responses may span hormone signalling, 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, uptake and conversion of VOCs and the adsorption of VOCs to plant surfaces is presented. This is followed by 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 effective evaluation of mechanisms and fitness consequences of receiver plant exposure to VOCs.
... Plants perceive and respond to complex blends of above-or belowground VOCs emitted by conspecific or heterospecific neighbouring plants, resulting in so-called "plant communication" (Heil & Karban, 2010;Karban et al., 2014). Specifically, studies have found full induction or priming of defences by "receiver" plants when exposed to incoming VOCs released by attacked neighbours ("emitters"), thus boosting their resistance against herbivory (reviewed by Karban, 2015). ...
... Specifically, studies have found full induction or priming of defences by "receiver" plants when exposed to incoming VOCs released by attacked neighbours ("emitters"), thus boosting their resistance against herbivory (reviewed by Karban, 2015). To date, plant communication has been documented in over 30 plant species, including several agricultural crops and tree species (Heil & Karban, 2010;Karban et al., 2014), and is now a wellaccepted form of airborne signalling influencing plant-induced defences. Moreover, its use in pest management (e.g., exogenous application of VOCs to induce resistance) has been proposed to boost plant protection and reduce pesticide use (Pickett & Khan, 2016;Stenberg et al., 2015;Turlings & Erb, 2018). ...
Article
• Plant communication via airborne volatile organic compounds is a widespread phenomenon by which volatile organic compounds from damaged plants boost herbivore resistance in receiver plants. This phenomenon has been studied only in a handful of crop species. • We tested for communication between potato (Solanum tuberosum) plants in response to herbivory by the Colorado potato beetle, Leptinotarsa decemlineata. For this, we performed a greenhouse experiment with 15 potato varieties for which we caged pairs of plants (i.e., emitters and receivers) of the same variety. Half of the emitter plants were subjected to leaf damage by beetle larvae and the other half remained intact. We collected volatile organic compounds from emitter plants and estimated L. decemlineata damage on receivers. • We found no evidence of quantitative (total production) or qualitative (compound composition) changes in volatile organic compound emissions due to beetle herbivory. In addition, the leaf damage treatment on emitters had no significant effect on receiver herbivore resistance, suggesting no communication between infested and non-infested potato plants in response to Colorado potato beetle damage. • Overall, this study provides baseline information on airborne signalling (or the lack of thereof) in potato plants which can inform subsequent work that identifies airborne volatiles with potentially strong effects on priming or defence induction.
... Plant volatiles can also modulate interactions between herbivores on different plants through indirect effects on plant physiology. Many reports have demonstrated that herbivore-induced plant volatiles may act as airborne cues that influence other plant species growing in the near vicinity, which respond to these chemicals by upregulating or priming their own defences in anticipation of possible herbivory (Engelberth et al. 2004;Erb et al. 2015;Karban et al. 2014;Ninkovic et al. 2020). The downstream physiological routes by which this occurs are complex and are both insect and plant-species dependent, but their expression commonly depends on more general cues that include plant phytohormones like ethylene, jasmonic and salicylic acid, and green leaf volatiles like aldehydes, alcohols, and terpenes (Karban 2015). ...
... This has been previously found in other specialist aphids that benefit from phytohormonal responses or plant defensive metabolites (Züst and Agrawal 2016). Plant responses to volatiles produced by other plant species have been documented in a number of other systems (Engelberth et al. 2004;Erb et al. 2015;Karban et al. 2014;Ninkovic et al. in press), though we are not aware of studies involving wheat. Insect responses to plant volatiles emitted by non-host plants are also well documented (Turlings and Erb 2018), but long-term multigenerational experiments exploring this question are scarce. ...
Article
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Many insect herbivores engage in apparent competition whereby two species interact through shared natural enemies. Upon insect attack, plants release volatile blends that attract natural enemies, but whether these volatiles mediate apparent competition between herbivores is not yet known. We investigate the role of volatiles that are emitted by bean plants upon infestation by Acyrthosiphon pisum aphids on the population dynamics and fitness of Sitobion avenae aphids, and on wheat phloem sap metabolites. In a field experiment, the dynamics of S. avenae aphids on wheat were studied by crossing two treatments: exposure of aphid colonies to A. pisum-induced bean volatiles and exclusion of natural enemies. Glasshouse experiments and analyses of primary metabolites in wheat phloem exudates were performed to better understand the results from the field experiment. In the field, bean volatiles did not affect S. avenae dynamics or survival when aphids were exposed to natural enemies. When protected from them, however, volatiles led to larger aphid colonies. In agreement with this observation, in glasshouse experiments, aphid-induced bean volatiles increased the survival of S. avenae aphids on wheat plants, but not on an artificial diet. This suggests that volatiles may benefit S. avenae colonies via metabolic changes in wheat plants, although we did not find any effect on wheat phloem exudate composition. We report a potential case of associational susceptibility whereby plant volatiles weaken the defences of receiving plants, thus leading to increased herbivore performance.
... Understanding the plant-insect interactions is of utmost importance for developing effective pest management approaches. Direct damage to the plant or exposure to volatiles results in induced resistance 8 . Induced defense responses compromise less plant fitness and are more durable as compared to constitutive defense mechanisms 9 . ...
Article
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Pink stem borer (PSB) causes considerable yield losses to maize. Plant–insect interactions have significant implications for sustainable pest management. The present study demonstrated that PSB feeding, mechanical wounding, a combination of mechanical wounding and PSB regurgitation and exogenous application of methyl jasmonate have induced phenolic compound mediated defense responses both at short term (within 2 days of treatment) and long term (in 15 days of treatment) in leaf and stalk tissues of maize. The quantification of two major defense related phenolic compounds namely p-Coumaric acid (p-CA) and ferulic acid (FA) was carried out through ultra-fast liquid chromatography (UFLC) at 2 and 15 days after imposing the above treatments. The p-CA content induced in leaf tissues of maize genotypes were intrinsically higher when challenged by PSB attack at V3 and V6 stages in short- and long-term responses. Higher p-CA content was observed in stalk tissues upon wounding and regurgitation in short- and long-term responses at V3 and V6 stages. Significant accumulation of FA content was also observed in leaf tissues in response to PSB feeding at V3 stage in long-term response while at V6 stage it was observed both in short- and long-term responses. In stalk tissues, methyl jasmonate induced higher FA content in short-term response at V3 stage. However, at V6 stage PSB feeding induced FA accumulation in the short-term while, wounding and regurgitation treatment-induced defense responses in the long-term. In general, the resistant (DMRE 63, CM 500) and moderately resistant genotypes (WNZ ExoticPool) accumulated significantly higher contents of p-CA and FA content than susceptible ones (CM 202, BML 6) in most of the cases. The study indicates that phenolic mediated defense responses in maize are induced by PSB attack followed by wounding and regurgitation compared to the other induced treatments. Furthermore, the study confirmed that induced defense responses vary with plant genotype, stage of crop growth, plant tissue and short and long-term responses. The results of the study suggested that the Phenolic acids i.e. p-CA and FA may contribute to maize resistance mechanisms in the maize-PSB interaction system.
... In response to damages caused by herbivorous arthropods, plants start emitting herbivory-induced plant volatiles (HIPVs) (Takabayashi and Shiojiri, 2019). When uninfested conspecific plants received HIPVs, they become more defensive against herbivores [for review see Karban et al. (2014) and Yoneya and Takabayashi (2016)]. Besides responding to HIPVs, plants also respond to volatiles from artificially damaged plants. ...
Article
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It is known that undamaged plants that have been exposed to volatiles from damaged con- or heterospecific plants become more resistant against herbivores. This is one of the plants’ induced resistant responses against herbivores. To test whether this response can be used for rice production, we conducted the following experiments over 2 years (2012 and 2013). Rice seedlings were first planted in the rice seedling bed for 2 weeks in early May. There, half of the rice seedlings were exposed to artificially damaged weed volatiles three times for 12 days (treated plants). Weeds were randomly collected from the areas that were >100 m away from the seedling bed and the rice paddy fields. The remaining seedlings were not exposed (control plants). In the middle of May, bunches (ca. three seedlings per bunch) were transplanted to the rice paddy field. In July, leaf damage was observed. The total number of leaves in the treated and control plants was not significantly different. In contrast, the total number of damaged leaves in the treated plants was significantly lower than that in the control plants. In September, rice grains were harvested. The average weight of a rice grain from the treated and control plants was not significantly different. However, the weight of grains per bunch of treated plants was significantly higher than that of control plants; this indicated a significant increase of the number of grains by 23% in 2012 and by 18% in 2013 in the treated plants compared to that in the control plants. The volatiles emitted from the weeds included monoterpenoids (40.4% in total), green leaf volatiles (46.5%), short-chain alcohols (5.3%), short-chain ketone (5.4%), short-chain acetate (0.5%), short-chain aldehyde (1.1%), and hydrocarbon (0.7%). These results suggest that exposure of volatiles from artificially damaged weeds to rice seedlings has the potential to increase rice production.
... From earlier studies we know that winter browsing by red deer on bilberry did not result in the same systematic plant responses indicative of induced defences as did chemical treatment . Most studies of induced plant defences point to herbivory by insects as the main inducer of plant resistance (Howe & Jander, 2008;Karban, Yang & Edwards, 2014), and even if ungulate browsing may modify plant quality it may be by other mechanisms than induced defences. ...
Article
Ecological theory predicts the strongest ecosystem effects of herbivory when dominant and ecologically important species are consumed. Bilberry, Vaccinium myrtillus, is such a key plant species, attractive to many other species in the boreal forests, for example ungulate and invertebrate herbivores. Large herbivores may remove substantial biomass and alter plant quality and therefore affect abundance and populations of invertebrate animals sharing the same food plant. We combined experimental exclusion of ungulates with a browsing intensity gradient to investigate the 15-year effect of ungulate (Cervus elaphus and Ovis aries) browsing on bilberry plant size and on bilberry-feeding herbivorous larvae (Lepidoptera and Symphyta), in a Norwegian old growth boreal forest ecosystem. Bilberry ramets in exclosure plots had nearly nine times higher dry mass and three times higher abundance of invertebrates feeding on them than in ungulate-access plots. Sweep-netting data verified these findings as larval numbers were twice as high in exclosure plots. The pattern in the large herbivore effects on bilberry size and abundance of herbivorous larvae were identical along the browsing gradient. Differences in larval abundance between treatments, as indicated by leaf-chewing, increased during the 15-year study period, and the community fluctuations were larger when ungulate herbivores were excluded. The browsing effect was moderated by plant quality as larval densities were lowest on both heavily-browsed and non-browsed plants, and highest on ramets that had 50-74% of annual shoots browsed. Our study supports previous findings in that bilberry is relatively disturbance tolerant and may recover quickly, and that ungulates may compete with herbivorous larvae for food biomass. Additionally, our results strongly indicated that population insect community peaks and fluctuations are dampened by ungulate consumption. Our findings add to the understanding on how ungulates may structure forest ecosystems directly and indirectly.
... Its release into the air constitutes a volatile defence signal that activates the resistance of neighbouring tobacco plants (Shulaev et al., 1997). Karban et al. (2014), who combined the results of 48 studies, confirmed the existence of "chemical communication" between plants. MeSA is therefore an indicator of diseased plants (Jansen et al., 2011) and has been evidenced as biomarker of grapevine leaves infected with downy mildew caused by Plasmopara viticola (Chalal et al., 2015). ...
Article
Methyl salicylate (MeSA) is a plant metabolite that induces plant defence resistance and an odorous volatile compound presenting green nuances. This volatile compound was shown to be present in wine samples, sometimes at concentrations above its olfactory detection threshold. MeSA is localized in grapes, particularly in the skins and stems, and is extracted during red wine vinification. It was detected at the highest concentrations in wines of several grape varieties, made from grapes affected by cryptogamic diseases, namely downy mildew caused by Plasmopara viticola, and black rot caused by Guignardia bidwellii. It has also been detected in wines from vines affected by Esca, a Grapevine Trunk Disease. MeSA can also be considered to be a chemical marker in grapes and wine indicative of the level of development of several vine cryptogamic diseases.
... Recognition of these airborne chemicals in turn triggers molecular and physiological cascades that can induce trait changes related to resistance. Intriguingly, there is evidence that other plants (of the same or different species) may "eavesdrop" on such chemical signals, exhibiting trait changes in response to perceived enemy risk (reviews by Karban et al., 2014;Ameye et al., 2018;Bouwmeester et al., 2019). For example, undamaged, neighboring lima bean plants were able to recognize HIPVs from attacked plants, activating a defensive response in the form of extra-floral nectaries to attract enemies of herbivores (Kost and Heil, 2006). ...
Article
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Predators kill and consume prey, but also scare living prey. Fitness of prey can be reduced by direct killing and consumption, but also by non-consumptive effects (NCEs) if prey show costly risk-induced trait responses (RITRs) to predators, which are meant to reduce predation risk. Recently, similarities between predators and parasites as natural enemies have been recognized, including their potential to cause victim RITRs and NCEs. However, plant-herbivore and animal host-parasite associations might be more comparable as victim-enemy systems in this context than either is to prey-predator systems. This is because plant herbivores and animal parasites are often invertebrate species that are typically smaller than their victims, generally cause lower lethality, and allow for further defensive responses by victims after consumption begins. Invertebrate herbivores can cause diverse RITRs in plants through various means, and animals also exhibit assorted RITRs to increased parasitism risk. This synthesis aims to broadly compare these two enemy-victim systems by highlighting the ways in which plants and animals perceive threat and respond with a range of induced victim trait responses that can provide pre-emptive defense against invertebrate enemies. We also review evidence that RITRs are costly in terms of reducing victim fitness or abundance, demonstrating how work with one victim-enemy system can inform the other with respect to the frequency and magnitude of RITRs and possible NCEs. We particularly highlight gaps in our knowledge about plant and animal host responses to their invertebrate enemies that may guide directions for future research. Comparing how potential plant and animal victims respond pre-emptively to the threat of consumption via RITRs will help to advance our understanding of natural enemy ecology and may have utility for pest and disease control.
... Frequently, a single host plant is exploited concurrently by several herbivore species belonging to different guilds, which create additional attracting or repelling cues. The emission of volatile compounds is perhaps the most studied of these cues (see Karban et al. 2014). Co-occurrence of herbivores, for instance, has been reported in super-host plants, which support several species of galling insect simultaneously (e.g. ...
Article
• Host plant selection by herbivores is driven by a complex array of cues, including leaf traits and previous leaf damage. Herbivore-associated cues to host selection at the plant and leaf scale aid understanding of mechanisms responsible for host preference that might translate into increased performance, as well as processes structuring herbivore populations mediated by interactions. We investigated how changes induced by a galling insect in the tropical fern Cyathea phalerata act as repellent or attractant cues for sawfly feeding and the effects of leaf size on herbivory levels. • We recorded gall abundance, damage by chewers, leaf size, plant nutritional quality, phenolic concentration and leaf anatomical traits between galled and non-galled leaf samples. • Galled samples contained less N, higher levels of phenolics and higher C/N ratio. However, leaf-chewing damage did not differ between galled and non-galled leaves. The gall structure was avoided by chewers, as it had high concentrations of phenolics, lignification and suberization. Larger leaves sustained higher gall abundance, but leaf size did not have a significant effect on chewer damage. A co-occurrence index calculated for both guilds indicated that galls and chewers exhibited a distribution that did not differ from random, reinforcing that the two guilds on C. phalerata do not show patterns of repulsion such as those maintained by interspecific competition. • Sawflies dismissing chemical cues indicate that the increase in phenolics caused by galling insects does not generate increased protection of the galled pinnules. Our results highlight ferns as key resources for herbivores and as a potential plant group to study new research avenues on plant–insect interactions.
... These compounds may, for instance, protect plants against biotic and abiotic stresses [12][13][14]. VOCs can also include defense mechanisms to control growth of neighboring plants [15]. The aroma of wine is one of the main factors that determines its quality, and derives from both the VOCs present in the berries [16], and those produced during the fermentation and aging [17,18]. ...
Article
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Abscisic acid (ABA) plays a crucial role in the plant responses to environmental signals, in particular by triggering secondary metabolism. High-altitude vineyards in Mendoza, Argentina, are exposed to elevated solar ultraviolet-B (UV-B) levels and moderate water deficits (WD), thus producing grapevine berries with high enological quality for red winemaking. Volatile organic compounds (VOCs) and phenolic compounds (PCs) accumulate in the berry skins, possess antioxidant activity, and are important attributes for red wine. The aim of the present study was to analyze the role of ABA in the modulation of these compounds in Vitis vinifera L. cv. Malbec wines by comparing the independent and interactive effects of UV-B, WD, and ABA. Two UV-B treatments (ambient solar UV-B or reduced UV-B), two watering treatments (well-watered or moderate water deficit) and two ABA treatments (no ABA and sprayed ABA) were given in a factorial design during one growing season. Sprayed ABA, alone and/or in combination with UV-B (specially) and WD (to a lower degree) increased low molecular weight polyphenols (LMWP), anthocyanins, but most noticeably the stilbenes trans-resveratrol and piceid. Under these treatments, VOCs were scarcely affected, and the antioxidant capacity was influenced by the combination of UV-B and WD. From a technological point of view, ABA applications may be an effective vineyard management tool, considering that it elicited a higher content of compounds beneficial for wine aging, as well compounds related to color.
... A bee will perform her waggle dance to encode certain specific information that may easily be decoded by observing bees who share the bee-code. 17 All across the animal kingdom (and arguably in parts of the plant world too, see: Karban, Yang and Edwards, 2014;Manusco, 2018), communication is achieved in this way. What is essential for this code-based communication to work, is that the signifier remains consistently wedded to the signified. ...
Thesis
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A central diagnostic and anecdotal feature of autism is difficulty with social communication. Traditionally, these difficulties are regarded as autistic impairments, related to proposed cognitive and social deficits. From this perspective the onus of failures in mutual understanding is placed within the mind/brains of the autistic individuals involved. However, recent research in the social sciences and critical autism studies is beginning to demonstrate that non-autistic people have challenges in understanding autistic people too, and to reframe the communicative difficulties as a two-way double empathy problem. A survey of the literature reveals the need for further empirical investigation of the proposed double empathy problem. This thesis builds on contemporary studies examining intersubjectivity between autistic and non-autistic people, and moves this research into the domain of cognitive linguistics. It explores, theoretically, whether relevance theory (a cognitive account of utterance interpretation) might help make sense of what is happening pragmatically during these breakdowns in mutual understanding. It also examines whether a radical reframing of these breakdowns as akin to intercultural problems might provide any valuable insights. The thesis begins with an interdisciplinary literature review that outlines the central constructs and themes contained within. To begin, the thesis presents an overview of autism research, covering both traditional biomedical theories and more recent phenomenological perspectives informed by the neurodiversity paradigm. Autistic minds are considered as autistically embodied agents navigating a social world comprised of non-autistically shaped norms. Relevance theory is then introduced within the wider context of cognitive pragmatics, and its application to interactions across dispositional borders (i.e. between autistic and non-autistic individuals) technically explored. The second half of the thesis reports on and discusses the results of a small-scale linguistic ethnographic case study. Eight core autistic participants engaged in three naturalistic conversations around the topic of loneliness with; (1) a familiar, chosen conversation partner; (2) a non-autistic stranger and (3) an autistic stranger. Relevance theory is utilized as a frame for the linguistic analysis of the interactions to investigate where mutual understanding is and is not achieved. There is increasing acknowledgement of the importance of autistic stakeholder involvement in autism research. In order to bring my own autistic insights more centrally into this work, I have taken an autoethnographic approach. This method draws on the lived experience of the researcher as a member of the group being studied, and as such offers an emancipatory mechanism for raising up previously marginalized voices.
... However, pest management by genetic manipulation of volatiles in the plant is not always successful in the field due to its complex context-dependency (Bruce et al., 2015). In another line of defense, plants communicate danger signals to other plants (Karban et al., 2006;Karban et al., 2014;Kalske et al., 2019). For example, the volatile homoterpene compound (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) mediates plant-plant communication in sweet potato (Ipomoea batatas) and triggers systemic and jasmonic acid (JA)-independent anti-herbivore defenses in neighboring plants. ...
Article
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Insect pests negatively affect crop quality and yield; identifying new methods to protect crops against insects therefore has important agricultural applications. Our analysis of transgenic Arabidopsis thaliana plants showed that overexpression of PENTACYCLIC TRITERPENE SYNTHASE 1 ( PEN1 ), encoding the key biosynthetic enzyme for the natural plant product (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), led to significant resistance against a major insect pest, Plustella xylostella . DMNT treatment severely damaged the peritrophic matrix (PM), a physical barrier isolating food and pathogens from the midgut wall cells. DMNT repressed the expression of PxMucin in midgut cells and knocking down PxMucin resulted in PM rupture and P. xylostella death. A 16S RNA survey revealed that DMNT significantly disrupted midgut microbiota populations and that midgut microbes were essential for DMNT-induced killing. Therefore, we propose that the midgut microbiota assists DMNT in killing P. xylostella . These findings may provide a novel approach for plant protection against P. xylostella .
... It cannot be completely ruled out that volatiles released by the nearby leek plant could have directly enhanced induced sweet pepper defense mechanisms toward M. persicae. Certain VOCs have been shown to stimulate neighboring plants to adjust their defenses at the right time and subsequently reduce herbivore feeding damages [45][46][47] . The physiological studies were carried out both in clip-cages and in Petri dishes. ...
Article
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Combining a non-host plant (companion plant or CP) with a target cultivated plant is considered as a promising strategy to reduce pest pressure. Among the companion plants (CP) commonly used in integrated systems, those belonging to the Amaryllidaceae family (chives, garlic, onion, leek) exhibit characteristics related to certain volatile organic compounds (VOCs) with promising repellent potentialities. The aim of this work was to investigate the potential disruption of sweet pepper (host plant) colonization by the green peach aphid (Myzus persicae) when exposed to leek (Allium porrum) as a CP. Retention/dispersion, EPG and clip-cage/Petri dish laboratory experiments were thus performed to study the effect of leek VOCs on aphid settlement/migration, feeding behavior and life history traits parameters, respectively. This work revealed that leek as a CP had a negative effect on aphid feeding behavior, by disturbing the balance between phloem and xylem sap ingestion, but had no influence concerning aphid settlement. Surprisingly, leek as a CP triggered some unexpected probiotic effects on certain life history traits such as aphid survival, biomass, and fecundity, suggesting a possible hormetic effect of leek VOCs on aphid physiology. The possibility of experience-induced preference of aphids for leek VOCs was also discussed.
... This scepticism occurred despite the well-known facts that plants can sense and respond to the presence of other plants, for example, through light signals (Pierik & de Wit, 2014) and physical contact (de Wit et al., 2012). Plants can even detect the status of neighbours, for example, whether a neighbour is attacked by a herbivore being conveyed through volatiles (Karban, Yang, & Edwards, 2014) or whether the neighbour is stressed by drought being conveyed through sounds (Jeong et al., 2014). The fact that plants can distinguish between self-and non-self, and are thus capable of some level of identity recognition, has been evident from the observation that many species prevent self-pollination (Fujii, Kubo, & Takayama, 2016). ...
Article
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The phenomenon that organisms can distinguish genetically related individuals from strangers (i.e. kin recognition) and exhibit more cooperative behaviors towards their relatives (i.e. positive kin discrimination) has been documented in a wide variety of organisms. However, its occurrence in plants has only been recently considered. Despite the concerns about some methodologies used to document kin recognition, there is sufficient evidence to state that it exists in plants. Effects of kin recognition go well beyond reducing resource competition between related plants, and involve interactions with symbionts (e.g. mycorrhizal networks). Kin recognition thus likely has important implications for evolution of plant traits, diversity of plant populations, ecological networks and community structures. Moreover, as kin selection may result in less competitive traits and thus greater population performance, it holds potential promise for crop breeding. Exploration of these evo‐ecological and agricultural implications requires: adequate control for‐ and measurements of relatedness, sufficient replication at genotypic level and comprehensive measurements of performance/fitness effects of kin discrimination. The primary questions that need to be answered are: when, where and by how much positive kin discrimination improves population performance. This article is protected by copyright. All rights reserved.
... Volatiles Volatiles from damaged neighbours increase resistance against herbivores across plant species [92] The parasitic plant fiveangled dodder (Cuscuta pentagona) exhibits directed growth toward volatiles of the potential plant host [93] Nonvolatile exudates Root-secreted JA is involved in neighbour detection and plant-plant communication in common wheat (Triticum aestivum) ...
Article
To achieve ecological and reproductive success, plants need to mitigate a multitude of stressors. The stressors encountered by plants are highly dynamic but typically vary predictably due to seasonality or correlations among stressors. As plants face physiological and ecological constraints in responses to stress, it can be beneficial for plants to evolve the ability to incorporate predictable patterns of stress in their life histories. Here, we discuss how plants predict adverse conditions, which plant strategies integrate predictability of biotic stress, and how such strategies can evolve. We propose that plants commonly optimise responses to correlated sequences or combinations of herbivores and pathogens, and that the predictability of these patterns is a key factor governing plant strategies in dynamic environments.
... phytophagous insects in over 30 plant species, including agricultural crops and tree species (Heil & Karban, 2010;Karban et al., 2014), and is now recognized as an important (and potentially widespread) modulator of plant defensive responses and induced resistance. ...
Article
Plant communication in response to insect herbivory has been increasingly studied, whereas that involving pathogen attack has received much less attention. We tested for communication between potato (Solanum tuberosum) plants in response to leaf infection by the fungal pathogen Sclerotinia sclerotiorum. To this end, we measured the total amount and composition of volatile organic compounds (VOCs) produced by control and infected emitter plants, as well as tested for induced resistance of receiver plants exposed to VOCs from emitters. We further tested for changes in the expression of defensive genes due to pathogen infection. Fungal infection did not significantly affect the total amount or composition of VOCs produced by emitter plants. Correspondingly, we found no evidence of higher resistance to the pathogen in receiver plants exposed to VOCs from infected emitters relative to control emitters. Molecular analyses indicated that pathogen infection drove a down‐regulation of genes coding for VOC precursors, potentially explaining the absence of pathogen effects on VOC emissions and thus of communication. Overall, these results indicate no evidence of airborne communication between potato plants in response to fungal infection and point at pathogen inhibition of VOC emissions as a likely explanation for this result.
... We confirmed that the attractant did not affect the oviposition behaviour of DBM adults on mizuna plants (the number of eggs), the pupation rate and the pupal weight of DBM larvae on mizuna plants (electronic supplementary materials and figure S2). Thus, in contrast with other studies [28][29][30][31][32][33][34], the attractant did not affect the performance of either DBM adults or larvae. We could therefore focus solely on the C. vestalis-attracting function of the HIPV dispensers. ...
Article
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We investigated the recruitment of specific parasitoids using a specific blend of synthetic herbivory-induced plant volatiles (HIPVs) as a novel method of pest control in greenhouses. In the Miyama rural area in Kyoto, Japan, diamondback moth (DBM) ( Plutella xylostella , Lepidoptera: Plutellidae) larvae are an important pest of cruciferous crops in greenhouses, and Cotesia vestalis (Hymenoptera: Braconidae), a larval parasitoid of DBM, is found in the surrounding areas. Dispensers of HIPVs that attracted C. vestalis and honey feeders were set inside greenhouses (treated greenhouses). The monthly incidence of DBMs in the treated greenhouses was significantly lower than that in the untreated greenhouses over a 2-year period. The monthly incidences of C. vestalis and DBMs were not significantly different in the untreated greenhouses, whereas monthly C. vestalis incidence was significantly higher than monthly DBM incidence in the treated greenhouses. Poisson regression analyses showed that, in both years, a significantly higher number of C. vestalis was recorded in the treated greenhouses than in the untreated greenhouses when the number of DBM adults increased. We concluded that DBMs were suppressed more effectively by C. vestalis in the treated greenhouses than in the untreated greenhouses.
... This population-specific effect was found in both of the sites where the experiments were conducted showing that cues vary geographically in their effectiveness and suggesting that sagebrush has a stronger response to local than to foreign dialects. The investigators also observed that the volatiles emitted by damaged sagebrush plants were characterized into two heritable chemotypes (dominated by either thujone or camphor) and that following leaf damage, individuals of the same chemotype communicated more effectively than individuals of differing chemotypes [96,97]. These findings seem to indicate that chemotypes can be considered examples of language differences based on relatedness, suggesting that language is shaped by the context in which it is used and in which it develops [84]. ...
Article
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The linguistic behavior of humans is usually considered the point of reference for studying the origin and evolution of language. As commonly defined, language is a form of communication between human beings; many have argued that it is unique to humans as there is no apparent equivalent for it in non-human organisms. How language is used as a means of communication is examined in this essay from a biological perspective positing that it is effectively and meaningfully used by non-human organisms and, more specifically, by plants. We set out to draw parallels between some aspects characterizing human language and the chemical communication that occurs between plants. The essay examines the similarities in ways of communicating linked to three properties of language: its combinatorial structure, meaning-making activities and the existence of dialects. In accordance with the findings of researchers who have demonstrated that plants do indeed communicate with one another and with organisms in their environment, the essay concludes with the appeal for an interdisciplinary approach conceptualizing a broader ecological definition of language and a constructive dialogue between the biological sciences and the humanities.
... Thus, the altered acceptance of the host plant by brushed geranium VOCs is likely to be the consequence of aphid intoxication by inhalation by germacrone and β-elemenone. Finally, certain VOCs have also been shown to stimulate neighboring plants to adjust their defenses at the right time and subsequently reduce herbivore feeding damages as demonstrated in several studies (Karban et al. 2014;Ninkovic et al. 2019;Tolosa et al. 2019). ...
Article
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The combination of a companion plant with a cultivated plant is considered an interesting strategy to reduce pest pressure and, hence, the use of pesticides. Although several plants from the Alliaceae and Lamiaceae families are known to be efficient companion plants against aphid pests, only a few plants of the Geraniaceae family have been studied so far. The aim of this work was to investigate the potential effects of Geranium macrorrhizum as a companion plant on the colonization of sweet pepper (Capsicum annuum, Solanaceae) by the green peach aphid (Myzus persicae). Aphid's orientation behavior, probing behavior and life history traits were assessed on sweet pepper using a host choice preference setup, Electrical Penetration Graph technique and clip-cage laboratory bioassays, respectively. The potential disturbance through mechanical stimulation of geranium leaves was also assessed. The composition of VOCs from G. macrorrhizum leaves was analyzed using SPME technic followed by GC-MS. This study revealed that G. macrorrhizum as a companion plant was intrinsically repellent but not enough to completely mask the attractive odor of the sweet pepper host plant. Moreover, G. macrorrhizum negatively impacted the probing behavior, fecundity and survival rate of M. persicae on sweet pepper. The effects were exacerbated when G. macrorrhizum leaves were mechanically stimulated. This could be due to the greater amount of the main VOCs germacrone and β-elemenone emitted by G. macrorrhizum following mechanical stimulation. Our results bring new insights into the use of novel companion plants to regulate aphid pest populations.
... Naturally occurring environmental stimuli that may reliably indicate impending herbivory and prime plants for improved defense against attack by herbivorous arthropods are, for example, volatile compounds released by herbivorous insects or by herbivore-infested plants. Exposure of plants to insect sex pheromones (Helms et al., 2014(Helms et al., , 2017Bittner et al., 2019), to herbivory-induced plant volatiles (HIPVs, e.g., Heil and Kost, 2006;Dicke and Baldwin, 2010;Karban et al., 2014), or to insect OIPVs (Pashalidou et al., 2020) has been shown to render a plant's anti-herbivore defense more effective. Furthermore, herbivory preceding further herbivory (e.g., Rasmann et al., 2012) and insect egg deposition preceding larval feeding damage Fatouros, 2015, 2016) are known to enhance plant defenses against the feeding stages of the herbivores. ...
Article
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Plants can respond to eggs laid by herbivorous insects on their leaves by preparing (priming) their defense against the hatching larvae. Egg-mediated priming of defense is known for several plant species, including Brassicaceae. However, it is unknown yet for how long the eggs need to remain on a plant until a primed defense state is reached, which is ecologically manifested by reduced performance of the hatching larvae. To address this question, we used Arabidopsis thaliana, which carried eggs of the butterfly Pieris brassicae for 1–6 days prior to exposure to larval feeding. Our results show that larvae gained less biomass the longer the eggs had previously been on the plant. The strongest priming effect was obtained when eggs had been on the plant for 5 or 6 days, i.e., for (almost) the entire development time of the Pieris embryo inside the egg until larval hatching. Transcript levels of priming-responsive genes, levels of jasmonic acid-isoleucine (JA-Ile), and of the egg-inducible phytoalexin camalexin increased with the egg exposure time. Larval performance studies on mutant plants revealed that camalexin is dispensable for anti-herbivore defense against P. brassicae larvae, whereas JA-Ile – in concert with egg-induced salicylic acid (SA) – seems to be important for signaling egg-mediated primed defense. Thus, A. thaliana adjusts the kinetics of its egg-primed response to the time point of larval hatching. Hence, the plant is optimally prepared just in time prior to larval hatching.
... The interaction between plants and arthropod herbivores is a complex molecular event where both parts try to ensure their survivability. Plants use cues emitted by herbivores such as sex pheromones (Helms et al., 2017) or even volatiles from neighboring damaged plants (Karban et al., 2014;Pashalidou et al., 2020), and prepare their defenses for future attacks. Among these cues, herbivore eggs induce several defense responses in many plant species (Gouhier-Darimont et al., 2013;Fatouros et al., 2014;Bittner et al., 2017;Geuss et al., 2017). ...
Article
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Herbivore oviposition produces all sorts of responses in plants, involving wide and complex genetic rearrangements. Many transcriptomic studies have been performed to understand this interaction, producing a bulk of transcriptomic data. However, the use of many transcriptomic techniques across the years, the lack of comparable transcriptomic context at the time of publication, and the use of outdated databases are limitations to understand this biological process. The current analysis intends to retrieve oviposition studies and process them with up-to-date techniques and updated databases. To reduce heterogeneities, the same processing techniques were applied, and Arabidopsis was selected to avoid divergencies on plant taxa stress response strategies. By doing so, we intended to understand the major mechanisms and regulatory processes linked to oviposition response. Differentially expressed gene (DEG) identification and co-expression network-based analyses were the main tools to achieve this goal. Two microarray studies and three RNA-seq analyses passed the screening criteria. The collected data pertained to the lepidopteran Pieris brassicae and the mite Tetranychus urticae , and covered a timeline from 3 to 144 h. Among the 18, 221 DEGs found, 15, 406 were exclusive of P. brassicae (72 h) and 801 were exclusive for the rest of the experiments. Excluding P. brassicae (72 h), shared genes on the rest of the experiments were twice the unique genes, indicating common response mechanisms were predominant. Enrichment analyses indicated that shared processes were circumscribed to earlier time points, and after 24 h, the divergences escalated. The response was characterized by patterns of time-dependent waves of unique processes. P. brassicae oviposition induced a rich response that shared functions across time points, while T. urticae eggs triggered less but more diverse time-dependent functions. The main processes altered were associated with hormonal cascades [e.g., salicilic acid (SA) and jasmonic acid (JA)], defense [reactive oxygen species (ROS) and glucosinolates], cell wall rearrangements, abiotic stress responses, and energy metabolism. Key gene drivers of the identified processes were also identified and presented. The current results enrich and clarify the information regarding the molecular behavior of the plant in response to oviposition by herbivores. This information is valuable for multiple stress response engineering tools, among other applications.
... 1−3 These compounds also facilitate intraand inter-species plant associations, 4−6 for instance, herbivoreinduced plant volatiles are known to trigger defense responses in neighboring plants. 7 Plant root exudates can also have allelopathic effects on plants of different species and facilitate kin recognition to avoid competition, 8−10 in addition to influencing microbial diversity. 11 These abilities of plants to emit, perceive, and respond to signals in their environment can be utilized for a broad range of management against agricultural pests. ...
Article
Plant parasitic nematodes (PPNs) develop through three major stages in their life cycle: hatching, infection, and reproduction. Interruption of any of these stages can affect their growth and survival. We used screenhouse pot experiments, laboratory in vitro hatching and mortality assays, and chemical analysis to test the hypothesis that the non-host Asteraceae plant vegetable black-jack (Bidens pilosa) suppresses infection of the PPN Meloidogyne incognita in two susceptible Solanaceae host plants, tomato (Solanum lycopersicum) and black nightshade (S. nigrum). In intercrop and drip pot experiments, B. pilosa significantly reduced the number of galls and egg masses in root-knot nematode (RKN)-susceptible host plants by 3-9-fold compared to controls. Chemical analysis of the most bioactive fraction from the root exudates of B. pilosa identified several classes of compounds, including vitamins, a dicarboxylic acid, amino acids, aromatic acids, and a flavonoid. In in vitro assays, the vitamins and aromatic acids elicited the highest inhibition in egg hatching, whereas ascorbic acid (vitamin) and 2-hydroxybenzoic acid (aromatic acid) elicited strong nematicidal activity against M. incognita, with LC50/48 h values of 12 and 300 ng/μL, respectively. Our results provide insights into how certain non-host plants can be used as companion crops to disrupt PPN infestation.
... A plant's response to priming cues may result in faster, earlier or stronger inducible resistance to the herbivore Douma et al., 2017). A wide range of cues has been shown to prime plant resistance against herbivores, including several volatile compounds, among them feeding-induced plant volatiles (Kost and Heil, 2006;Frost et al., 2008;Arimura et al., 2010;Dicke and Baldwin, 2010;Karban et al., 2014), volatiles induced by insect egg depositions (Pashalidou et al., 2020) and volatile insect sex pheromones that prime defence against feeding herbivores (Helms et al., 2017) or against the herbivore's eggs (Bittner et al., 2019). In addition to these cues conveyed via air, there are others that are directly associated with the plant wound, i.e. damage-associated molecular patterns and oral larval secretions released into the plant wound that prime resistance against herbivory (e.g. ...
Article
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While traits of plant resistance to herbivory often change during ontogeny, it is unknown whether the primability of this resistance depends on the plant’s developmental stage. Resistance in non-flowering Arabidopsis thaliana against Pieris brassicae larvae is known to be primable by prior egg deposition on leaves. We investigated whether this priming effect is maintained in plants in the flowering stage. Larval performance assays revealed that flowering plants’ resistance to herbivory was not primable by egg deposition. Accordingly, transcriptomes of flowering plants showed almost no response to eggs. In contrast, egg deposition on non-flowering plants enhanced the expression of genes induced by subsequent larval feeding. Strikingly, flowering plants showed constitutively high expression levels of these genes. Larvae performed generally worse on flowering than on non-flowering plants, indicating that flowering plants constitutively resist herbivory. Furthermore, we determined the seed weight in regrown plants that had been exposed to eggs and larvae during the non-flowering or flowering stage. The non-flowering plants benefitted from egg-priming with a smaller loss in seed yield. The seed yield of flowering plants was unaffected by the treatments, indicating tolerance towards the larvae. Our results show that the primability of Arabidopsis’ anti-herbivore defences depends on the plant’s developmental stage.
... In response to damages caused by herbivorous arthropods, plants start emitting herbivory-induced plant volatiles (HIPVs) . When uninfested conspecific plants received HIPVs, they become more defensive against herbivores [for review see Karban et al. (2014) and Yoneya and Takabayashi (2016)]. Besides responding to HIPVs, plants also respond to volatiles from artificially damaged plants. ...
Book
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The objective of this Research Topic is to highlight recent progress, key advances, and future perspectives in manipulating plant defense against insect pests using bioactive chemicals.
... Moreover, predatory or parasitic natural enemy insects use HIPVs to search and locate prey or hosts [71,[76][77][78]. HIPVs are not only perceived and used by insects, but also recognized by neighboring homologous or heterogeneous plants to predict the attack of herbivorous insects and prepare for defense against potential insect pests [79,80]. ...
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Turnip mosaic virus (TuMV) is an important threat to the yield and quality of brassica crops in China, and has brought serious losses to brassica crops in the Far East, including China and the north. Aphids (Hemiptera, Aphidoidea) are the main mediators of TuMV transmission in field production, and not only have strong virus transmission ability (small individuals, strong concealment, and strong fecundity), but are also influenced by the environment, making them difficult to control. Till now, there have been few studies on the resistance to aphids in brassica crops, which depended mainly on pesticide control in agriculture production. However, the control effect was temporarily effective, which also brought environmental pollution, pesticide residues in food products, and destroyed the ecological balance. This study reviews the relationship among brassica crop–TuMV, TuMV–aphid, and brassica crop–aphid interactions, and reveals the influence factors (light, temperature, and CO2 concentration) on brassica crop–TuMV–aphid interactions, summarizing the current research status and main scientific problems about brassica crop–TuMV–aphid interactions. It may provide theoretical guidance for opening up new ways of aphid and TuMV management in brassica crops.
... Moreover, despite the direct effects of garlic EO on aphid and psyllid behavior, it cannot be completely ruled out that volatiles released by rubber septa could also have indirectly modified the insect feeding behavior by modifying the host-plant chemistry, and in particular by enhancing host-plant defense mechanisms. Certain VOCs stimulate neighboring plants to adjust their defenses at the right time and subsequently reduce feeding by herbivores (Karban et al., 2014;Ninkovic et al., 2019;Tolosa et al., 2019). A longer duration of xylem sap ingestion could be considered as an aphid stress indicator associated with induced plant defenses (Prado & Tjallingii, 1997;Sauge et al., 2002). ...
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Essential oils (EOs) are promising sources of effective bioactive compounds for insect pest control, especially in heavily treated agrosystems like orchards. Plants belonging to the Amaryllidaceae family – onion, garlic (Allium sativum L.), and others – present an interesting potential in apple (Malus domestica Borkh.) and pear (Pyrus communis L., both Rosaceae) tree integrated pest management due to the repellent and deterrent properties of their chemical compounds. This study explores the potential disruption by garlic EOs of the behavior of two hemipteran pests towards their host trees: rosy apple aphid, Dysaphis plantaginea (Passerini) (Aphididae), on cultivated apple, and pear psyllid, Cacopsylla pyri (L.) (Psyllidae), on pear. Effects on orientation and feeding behavior were evaluated using choice tests and the electropenetrography (EPG) technique. The results revealed that garlic EOs delivered through rubber dispensers was intrinsically repellent, but when combined with the attractive host plant, the repellents and attractants canceled each other out for the two studied Hemiptera. Garlic EOs caused disruptions in the feeding behavior of the two insects, particularly the psyllids, which showed a decrease in phloem sap intake. This study highlights the mechanisms disrupting the process of host‐plant colonization, in particular the possible masking of host‐locating cues or the involvement of confusing chemical stimuli due to EO volatiles.
... The growing consciousness on the side effects of chemicals used for plant protection has resulted in increased research of more environment-friendly approaches, which encompass the manipulation (e.g., deterrence or repellence) of pest behaviour [45]. Such strategy has been investigated in several pest groups and can be either mediated by the plant through direct plant resistance or achieved using chemical compounds [46][47][48][49]. In our research, the oviposition deterrence efficacy of two new formulations was investigated, under field and laboratory conditions. ...
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The olive fruit fly, Bactrocera oleae, is the key pest of olive trees in several areas of the world. Given the need for the development of sustainable control methods, preventive tools, based on the manipulation of pest behaviour, must be considered. Here, under field and laboratory conditions, we tested the efficacy of different products in preventing B. oleae infestation. A field trial was conducted, from July to November 2020, in an olive orchard located in Central Italy. A table olive variety was selected and sprayed with rock powder, propolis, the mixture of both, copper oxychloride, or water (control). All treatments, except propolis, caused a reduction of B. oleae oviposition in olives, compared to the control. The mixture allowed the strongest reduction of fly infestation throughout the season, suggesting a synergistic effect. Behavioural no-choice assays were conducted to better understand the effects of treatments on B. oleae females. Compared to the control, females showed a lower preference for the central area of an arena containing an olive twig bearing two olive fruits, fully developed, but still green, treated with rock powder, plus propolis mixture. For all treatments, B. oleae showed lower oviposition events, suggesting deterrence to oviposition. Our results indicate that the tested products may have value against B. oleae, within integrated pest management (IPM) and organic agriculture.
... via abiotic processes, including those synthesized by humans, are used as indications of habitat quality or as navigational cues(Dittman and Quinn 1996, Hinojosa et al. 2018) Info-chemicals Local and possibly regional Biotic origin Indicates resource availability or presence of con-or hetero-specifics(Hay 2009) including reproductive status (Thomas 2011); trophic interactions/risk(Paterson et al. 2013, Karban et al. 2014; navigational cues (DeBose and Nevitt 2008) (Fig. genetic adaptation to ecosystem processes(Ousterhout et al. 2018, Abdala- Roberts et al. 2019; changes in population dynamics due to (mal)adaptation after alleles are introduced(Weeks et al. 2017, Kyriazis et al. 2021 ...
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Fluxes of matter, energy and information over space and time contribute to ecosystems' functioning and stability. The meta‐ecosystem framework addresses the dynamics of ecosystems linked by these fluxes but, to date, has focused solely on energy and matter. Here, we synthesize existing knowledge of information's effects on local and connected ecosystems and demonstrate how new hypotheses emerge from the integration of ecological information into meta‐ecosystem theory. We begin by defining information and reviewing how it flows among ecosystems to affect connectivity, local ecosystem function and meta‐ecosystem dynamics. We focus on the role of semiotic information: that which can reduce an individual's – or a group's – uncertainty about the state of the world. Semiotic information elicits behavioral, developmental and life history responses from organisms, potentially leading to fitness consequences. Organisms' responses to information can ripple through trophic interactions to influence ecosystem processes, their local and regional dynamics, and the spatiotemporal flows of energy and matter, therefore information should affect meta‐ecosystem dynamics such as stability and productivity. While specific subdisciplines of ecology currently consider different types of information (e.g. social and cultural information, natural and artificial light or sound, body condition, genotype and phenotype), many ecological models currently account for neither the spatio–temporal distribution of information nor its perception by organisms. We identify the empirical, theoretical and philosophical challenges in developing a robust information meta‐ecology and offer ways to overcome them. Finally, we present new hypotheses for how accounting for realistic information perception and responses by organisms could impact processes such as home range formation and spatial insurance, and thus our understanding of ecological dynamics across spatial and temporal scales. Accounting for information will be essential to understanding how dynamics such as fitness, organismal movement and trophic interactions influence meta‐ecosystem functioning, and predicting how ecosystem processes are affected by anthropogenic pressures.
... Evidence is not static and tends to change over time as a function of changes in research methods or characteristics of the subjects . For instance, meta-analyses on different ecological subjects found that the mean effect describing a relationship decreases with time, such as the impact of introduced species on native species richness (Crystal-Ornelas & Lockwood 2020), or the effect of volatile plant communication on herbivory (Karban et al. 2014). In a cumulative meta-analysis, a series of sequential meta-analyses are conducted, with studies ordered chronologically (Leimu & Koricheva 2004, Borenstein et al. 2009). ...
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• Mammals can influence ecosystem functioning through essential ecological processes. In patchy landscapes, mammalian diversity can be correlated with ecosystem productivity through its effect on resource availability. However, mammals comprise species with contrasting habitat use and requirements, and it is unknown whether the diversity–productivity relationship changes as a function of the mammal species’ traits. • We use meta-analytical techniques to quantify the effect and assess whether mammal species richness and abundance correlates positively with productivity. Further, we assess whether the diversity–productivity relationship is influenced by the species’ body mass (<1 kg: small, and >1 kg: large, and mixed small and large), the vertical strata explored by the species (terrestrial, arboreal, and mixed terrestrial and arboreal species), and the species’ feeding guild (herbivore, omnivore, insectivore, and mixed feeding guilds). • In total, 53 studies fitted the eligibility criteria worldwide, comprising 285 different effect sizes representing the magnitude of the mammal diversity–productivity relationship in six biogeographical realms. Ecosystem productivity was quantified with various surrogate variables, such as soil nutrients, annual rainfall, above-ground production, evapotranspiration, net primary production, plant cover, and elevation. • The relationships between productivity measures and both mammal species richness and abundance were significant and positive. Mammal diversity correlated positively with ecosystem productivity, for mammal species differing in body mass, the vertical strata explored by species (except arboreal mammals), and feeding guilds (except insectivorous mammals). Overall, this result supports the view that diversity in the entire mammal community is positively related to increasing productivity. • Sites with greater ecosystem productivity are usually associated with more resources and higher ecosystem carrying capacity, which provide greater resilience to human disturbance than less productive sites. Thus, quantifying productivity can help researchers to identify critical areas for restoration and to propose effective guidelines for mammal conservation.
... On the other hand, during the chemical transformation of ENMs in soil, a variety of different compounds are formed due to the release of metal ions from ENMs dissolution, which are adsorbed on the surface of soil particles. For instance, soft metals, such as Ag, Cu, Zn, etc., usually form metal sulfides due to their high tendency to form complexes with sulfur containing substances including bio-macromolecules and other inorganic-sulfur sediments present in the soil [159]. Hence, the life of different nanomaterials in various environments including soil varies with the inherent properties of ENMs and with various environmental factors [138]. ...
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A staggering number of nanomaterials-based products are being engineered and produced commercially. Many of these engineered nanomaterials (ENMs) are finally disposed into the soil through various routes in enormous quantities. Nanomaterials are also being specially tailored for their use in agriculture as nano-fertilizers, nano-pesticides, and nano-based biosensors, which is leading to their accumulation in the soil. The presence of ENMs considerably affects the soil microbiome, including the abundance and diversity of microbes. In addition, they also influence crucial microbial processes, such as nitrogen fixation, mineralization, and plant growth promoting activities. ENMs conduct in soil is typically dependent on various properties of ENMs and soil. Among nanoparticles, silver and zinc oxide have been extensively prepared and studied owing to their excellent industrial properties and well-known antimicrobial activities. Therefore, at this stage, it is imperative to understand how these ENMs influence the soil microbiome and related processes. These investigations will provide necessary information to regulate the applications of ENMs for sustainable agriculture and may help in increasing agrarian production. Therefore, this review discusses several such issues.
... The first hypothesis could explain the observed leaf mimicry without direct contact and is generally supported by the fact that volatile plant communication is widespread and multi-purpose 18 . Nonetheless, to our knowledge, there is no documented evidence of changes in leaf shape elicited by volatiles and, more importantly, known volatilemediated responses in receiver plants are rather general [18][19][20][21] , while leaf mimicry in Boquila is highly specific. The second hypothesis, the horizontal gene transfer (HGT) hypothesis, has been deemed implausible [22][23][24] . ...
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The mechanisms behind the unique capacity of the vine Boquila trifoliolata to mimic the leaves of several tree species remain unknown. A hypothesis in the original leaf mimicry report considered that microbial vectors from trees could carry genes or epigenetic factors that would alter the expression of leaf traits in Boquila. Here we evaluated whether leaf endophytic bacterial communities are associated with the mimicry pattern. Using 16S rRNA gene sequencing, we compared the endophytic bacterial communities in three groups of leaves collected in a temperate rainforest: (1) leaves from the model tree Rhaphithamnus spinosus (RS), (2) Boquila leaves mimicking the tree leaves (BR), and (3) Boquila leaves from the same individual vine but not mimicking the tree leaves (BT). We hypothesized that bacterial communities would be more similar in the BR–RS comparison than in the BT–RS comparison. We found significant differences in the endophytic bacterial communities among the three groups, verifying the hypothesis. Whereas non-mimetic Boquila leaves and tree leaves (BT–RS) showed clearly different bacterial communities, mimetic Boquila leaves and tree leaves (BR–RS) showed an overlap concerning their bacterial communities. The role of bacteria in this unique case of leaf mimicry should be studied further.
... These VOCs can also mediate disease resistance in neighboring plants. Many studies of plant-plant communication via VOCs have reported evidence of communication among neighboring plants that provides resistance to insects 8 . For example, plants growing near damaged neighboring plants become more resistant to herbivores than do those growing farther away, although most of the underlying associated physiological and genetic mechanisms remain unknown. ...
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Plants have developed sophisticated mechanisms to survive in dynamic environments. Plants can communicate via volatile organic compounds (VOCs) to warn neighboring plants of threats. In most cases, VOCs act as positive regulators of plant defense. However, the communication and role of volatiles in response to drought stress are poorly understood. Here, we showed that tea plants release numerous VOCs. Among them, methyl salicylate (MeSA), benzyl alcohol, and phenethyl alcohol markedly increased under drought stress. Interestingly, further experiments revealed that drought-induced MeSA lowered the abscisic acid (ABA) content in neighboring plants by reducing 9-cis-epoxycarotenoid dioxygenase ( NCED ) gene expression, resulting in inhibition of stomatal closure and ultimately decreasing early drought tolerance in neighboring plants. Exogenous application of ABA reduced the wilting of tea plants caused by MeSA exposure. Exposure of Nicotiana benthamiana to MeSA also led to severe wilting, indicating that the ability of drought-induced MeSA to reduce early drought tolerance in neighboring plants may be conserved in other plant species. Taken together, these results provide evidence that drought-induced volatiles can reduce early drought tolerance in neighboring plants and lay a novel theoretical foundation for optimizing plant density and spacing.
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1. Induced anti-herbivore defences in plants can shape ecosystem structure and functions. Since these are known to be highly variable, quantifying their sources of variation remains important to understand their eco-evolutionary roles. 2. We conducted meta-analysis of 647 experiments (paired control and treatment) from 192 studies to address sources of variation in induced anti-herbivore defensive traits. This covered different agents of herbivory (insect, mammal and clipping), studies in greenhouse and in field settings, and covered 24 types of defence traits in 163 species from 50 families across 24 angiosperm orders. We used meta-regression models—multi-level random-effects (MLREs) and robust variance estimators (RVEs)—to quantify variation due to study setting, herbivore type, chemical identity, angiosperm order, volatility, fertilization, and publication year as moderator variables. 3. There were strong indications for publication bias in favour of large effect sizes, and studies with adequate sample size and precision were rare. Strength of induction was distributed uniformly over the phylogeny of 24 angiosperm orders. Stronger effects were reported from greenhouses than in field conditions, and induction was uninfluenced by herbivore type. Volatiles showed stronger response than non-volatiles in greenhouses for insects. Biosynthetic precursors (e.g. jasmonates) and many defensive chemicals were induced in the greenhouse, but when measured in field conditions, they were unresponsive to herbivory and appear to be constitutive. Similar to constitutive response, induced responses were also unaffected by fertilization. Direction and magnitude of induction differ greatly from previous assessments as these have also changed over time, representing natural epistemological growth. A third of the variability was explained by moderators (marginal R^2: chemical identity, angiosperm order, study setting, herbivore type and publication year); another third (conditional R^2) was attributed to the identity of individual studies and observations. 4. Synthesis. Manipulative experiments reveal many intrinsic differences among defensive chemicals and traits. They suggest plants in greenhouses may respond very differently to herbivores from those in field conditions. Although biosynthetic pathways of chemical responses, their modes of action and their effects on herbivores are well-understood, studies with greater statistical power under ecologically relevant settings are needed to discern induced and constitutive defences in how plants respond to their natural enemies
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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.
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Since the early 1990s, ecologists and evolutionary biologists have aggregated primary research using meta-analytic methods to understand ecological and evolutionary phenomena. Meta-analyses can resolve long-standing disputes, dispel spurious claims, and generate new research questions. At their worst, however, meta-analysis publications are wolves in sheep's clothing: subjective with biased conclusions, hidden under coats of objective authority. Conclusions can be rendered unreliable by inappropriate statistical methods, problems with the methods used to select primary research, or problems within the primary research itself. Because of these risks, meta-analyses are increasingly conducted as part of systematic reviews, which use structured, transparent, and reproducible methods to collate and summarise evidence. For readers to determine whether the conclusions from a systematic review or meta-analysis should be trusted - and to be able to build upon the review - authors need to report what they did, why they did it, and what they found. Complete, transparent, and reproducible reporting is measured by 'reporting quality'. To assess perceptions and standards of reporting quality of systematic reviews and meta-analyses published in ecology and evolutionary biology, we surveyed 208 researchers with relevant experience (as authors, reviewers, or editors), and conducted detailed evaluations of 102 systematic review and meta-analysis papers published between 2010 and 2019. Reporting quality was far below optimal and approximately normally distributed. Measured reporting quality was lower than what the community perceived, particularly for the systematic review methods required to measure trustworthiness. The minority of assessed papers that referenced a guideline (~16%) showed substantially higher reporting quality than average, and surveyed researchers showed interest in using a reporting guideline to improve reporting quality. The leading guideline for improving reporting quality of systematic reviews is the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) statement. Here we unveil an extension of PRISMA to serve the meta-analysis community in ecology and evolutionary biology: PRISMA-EcoEvo (version 1.0). PRISMA-EcoEvo is a checklist of 27 main items that, when applicable, should be reported in systematic review and meta-analysis publications summarising primary research in ecology and evolutionary biology. In this explanation and elaboration document, we provide guidance for authors, reviewers, and editors, with explanations for each item on the checklist, including supplementary examples from published papers. Authors can consult this PRISMA-EcoEvo guideline both in the planning and writing stages of a systematic review and meta-analysis, to increase reporting quality of submitted manuscripts. Reviewers and editors can use the checklist to assess reporting quality in the manuscripts they review. Overall, PRISMA-EcoEvo is a resource for the ecology and evolutionary biology community to facilitate transparent and comprehensively reported systematic reviews and meta-analyses.
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Plant diversity has often been reported to decrease insect herbivory in plants. Of the numerous mechanisms that have been proposed to explain this phenomenon, how plant diversity influences plant defences via effects on growth has received little attention. In addition, plant diversity effects may be contingent on abiotic conditions (e.g. resource and water availability). Here, we used a long‐term experiment to explore the interactive effects of tree species composition and water availability on growth, direct (i.e. phenolics) and indirect (i.e. volatile organic compounds – VOCs) defences and leaf herbivory in Quercus ilex. We quantified herbivory by chewing insects, phenolic compounds and VOCs in Q. ilex trees growing in stands differing in tree species composition (Q. ilex, Q. ilex + Betula Pendula, Q. ilex + Pinus pinaster and Q. ilex + B. pendula + P. pinaster) and water availability (irrigated versus control). Both direct and indirect defences were affected by tree species composition, but such changes were not mediated by changes in tree stem diameter. Quercus ilex trees growing in stands with P. pinaster had the lowest concentration of both direct and indirect defences. Importantly, the effects of tree species composition on VOCs were exacerbated on irrigated blocks. Despite variation in defences, tree species composition did not affect herbivory in Q. ilex. Accordingly, we did not find any association between defences and insect herbivory. Our results suggest that changes in the micro‐environment rather than growth‐defence associations may mediate tree diversity effects on defences. In addition, reduced defensive investment in more diverse stands could negatively impact tree resistance masking the beneficial effects of species diversity at reducing insect herbivory.
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Animal biologists have recently focused on individual variation in behavioral traits and have found that individuals of many species have personalities. These are defined as consistent intraspecific differences in behaviors that are repeatable across different situations and stable over time. When animals sense danger, some individuals will alert neighbors with alarm calls and both calling and responding vary consistently among individuals. Plants, including sagebrush, emit volatile cues when they are attacked by herbivores and neighbors perceive these cues and reduce their own damage. We experimentally transferred volatiles between pairs of sagebrush plants to evaluate whether individuals showed consistent variation in their effectiveness as emitters and as receivers of cues, measured in terms of reduced herbivore damage. We found that 64% of the variance in chewing damage to branches over the growing season was attributable to the identity of the individual receiving the cues. This variation could have been caused by inherent differences in the plants as well as by differences in the environments where they grew and their histories. We found that 5% of the variance in chewing damage was attributable to the identity of the emitter that provided the cue. This fraction of variation was statistically significant and could not be attributed to the environmental conditions of the receiver. Effective receivers were also relatively effective emitters, indicating consistency across different situations. Pairs of receivers and emitters that were effective communicators in 2018 were again relatively effective in 2019, indicating consistency over time. These results suggest that plants have repeatable individual personalities with respect to alarm calls.
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One of the characteristic aspects of odour sensing in humans is the activation of olfactory receptors in a slightly different manner in response to different enantiomers. Here, we focused on whether plants showed enantiomer-specific response similar to that in humans. We exposed Arabidopsis seedlings to methanol (control) and (+)- or (−)-borneol, and found that only (+)-borneol reduced the root length. Furthermore, the root-tip width was more increased upon (+)-borneol exposure than upon (−)-borneol exposure. In addition, root-hair formation was observed near the root tip in response to (+)-borneol. Auxin signalling was strongly reduced in the root tip following exposure to (+)-borneol, but was detected following exposure to (−)-borneol and methanol. Similarly, in the root tip, the activity of cyclin B1:1 was detected on exposure to (−)-borneol and methanol, but not on exposure to (+)-borneol, indicating that (+)-borneol inhibits the meristematic activity in the root. These results partially explain the (+)-borneol-specific reduction in the root length of Arabidopsis. Our results indicate the presence of a sensing system specific for (+)-borneol in Arabidopsis.
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Plants can adjust defence strategies in response to signals from neighbouring plants attacked by aboveground herbivores. Whether similar responses exist to belowground herbivory remains less studied, particularly regarding the spatiotemporal dynamics of such belowground signalling. We grew the grass Agrostis stolonifera with or without root-feeding nematodes (Meloidogyne minor). Leachates were extracted at different distances from these plants and at different times after inoculation. The leachates were applied to receiver A. stolonifera plants, of which root, shoot, and total biomass, root/shoot ratio, shoot height, shoot branch number, maximum rooting depth and root number were measured 3 weeks after leachate application. Receiver plants allocated significantly more biomass to roots when treated with leachates from nematode-inoculated plants at early infection stages. However, receiver plants’ root/shoot ratio was similar when receiving leachates collected at later stages from nematode-infected or control plants. Overall, early-collected leachates reduced growth of receiver plants significantly. Plants recently infected by root-feeding nematodes can thus induce increased root proliferation of neighbouring plants through root-derived compounds. Possible explanations for this response include a better tolerance of anticipated root damage by nematodes or the ability to grow roots away from the nematode-infected soil. Further investigations are still needed to identify the exact mechanisms.
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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.
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Herbivore-induced plant volatiles prime neighboring plants to respond more strongly to subsequent attacks. However, the key volatiles that trigger this state and their priming mechanisms remain largely unknown. The tea geometrid Ectropis obliqua is one of the most devastating leaf-feeding pests of tea plants. Here, plant–plant communication experiments demonstrated that volatiles emitted from tea plants infested by E. obliqua larvae triggered neighboring plants to release volatiles that repel E. obliqua adult, especially mated females. Volatile analyses revealed that the quantity of eight volatiles increased dramatically when plants were exposed to volatiles emitted by infested tea plants, including (Z)-3-hexenol, linalool, α-farnesene, β-Ocimene, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT).The results of behavioral bioassays demonstrated that β-Ocimene strongly repelled mated E. obliqua females. Individual volatile compound exposure experiments revealed that (Z)-3-hexenol, linalool, α-farnesene, and DMNT triggered the emission of β-Ocimene from tea plants. Chemical inhibition experiments demonstrated that the emission of β-Ocimene induced by (Z)-3-hexenol, linalool, α-farnesene, and DMNT was dependent on Ca²⁺ and JA signaling. These findings help us to understand how E. obliqua moths respond to volatiles emitted from tea plants and provide new insight into volatile-mediated plant–plant interactions. They have potential significance for the development of novel insect and pest control strategies in crops This article is protected by copyright. All rights reserved.
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Plants communicate via the emission of volatile organic compounds (VOCs) with many animals as well as other plants. We still know little about how VOCs are perceived by receiving (eavesdropping) plants. Here we propose a multiple system of VOC perception, where stress-induced VOCs dock on odorant-binding proteins (OBPs) like in animals and are transported to as-yet-unknown receptors mediating downstream metabolic and/or behavioral changes. Constitutive VOCs that are broadly and lifelong emitted by plants do not bind OBPs but may directly change the metabolism of eavesdropping plants. Deciphering how plants listen to their talking neighbors could empower VOCs as a tool for bioinspired strategies of plant defense when challenged by abiotic and biotic stresses.
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The ability of many animals to recognize kin has allowed them to evolve diverse cooperative behaviours; such ability is less well studied for plants. Many plants, including Artemisia tridentata, have been found to respond to volatile cues emitted by experimentally wounded neighbours to increase levels of resistance to herbivory. We report that this communication was more effective among A. tridentata plants that were more closely related based on microsatellite markers. Plants in the field that received cues from experimentally clipped close relatives experienced less leaf herbivory over the growing season than those that received cues from clipped neighbours that were more distantly related. These results indicate that plants can respond differently to cues from kin, making it less likely that emitters will aid strangers and making it more likely that receivers will respond to cues from relatives. More effective defence adds to a growing list of favourable consequences of kin recognition for plants.
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cis-Jasmone, or (Z)-jasmone, is well known as a component of plant volatiles, and its release can be induced by damage, for example during insect herbivory. Using the olfactory system of the lettuce aphid to investigate volatiles from plants avoided by this insect, (Z)-jasmone was found to be electrophysiologically active and also to be repellent in laboratory choice tests. In field studies, repellency from traps was demonstrated for the damson-hop aphid, and with cereal aphids numbers were reduced in plots of winter wheat treated with (Z)-jasmone. In contrast, attractant activity was found in laboratory and wind tunnel tests for insects acting antagonistically to aphids, namely the seven-spot ladybird and an aphid parasitoid. When applied in the vapor phase to intact bean plants, (Z)-jasmone induced the production of volatile compounds, including the monoterpene (E)-β-ocimene, which affect plant defense, for example by stimulating the activity of parasitic insects. These plants were more attractive to the aphid parasitoid in the wind tunnel when tested 48 h after exposure to (Z)-jasmone had ceased. This possible signaling role of (Z)-jasmone is qualitatively different from that of the biosynthetically related methyl jasmonate and gives a long-lasting effect after removal of the stimulus. Differential display was used to compare mRNA populations in bean leaves exposed to the vapor of (Z)-jasmone and methyl jasmonate. One differentially displayed fragment was cloned and shown by Northern blotting to be up-regulated in leaf tissue by (Z)-jasmone. This sequence was identified by homology as being derived from a gene encoding an α-tubulin isoform.
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The effects of defoliation of alder (Alnus glutinosa) on subsequent herbivory by alder leaf beetle (Agelastica alni) were studied in ten alder stands in northern Germany. At each site, one tree was manually defoliated (c. 20% of total foliage) to simulate herbivory. Subsequent damage by A. alni was assessed on ten alders at each site on six different dates from May to September 1994. After defoliation, herbivory by A. alni increased with distance from the defoliated tree. Laboratory experiments supported the field results. Not only leaf damage in the field, but also the extent of leaf consumption in laboratory feeding-preference tests and the number of eggs oviposited per leaf in another laboratory test were positively correlated with distance from the defoliated tree. Resistance was therefore induced not only in defoliated alders, but also in their undamaged neighbours. Consequently, defoliation of alders may trigger interplant resistance transfer, and therefore reduce herbivory in whole alder stands.
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Plants are capable of acquiring information from other plants, but are they able to send signals and communicate with them? Evolutionary biologists define biological communication as information transmission that is fashioned or maintained by natural selection and signals as traits whose value to the signaler is that they convey information to receivers. Plants, then, can be said to communicate if the signaling plant derives a fitness benefit from conveying information to other plants. Examples for interplant communication that fit these definitions potentially include territorial root communications, self/non-self recognition between roots and associated with self-incompatibility, volatile signals that induce defenses against herbivores, signals from ovules to mother plants, signals associated with root graft formation, and male to female signals during pollen competition. Natural selection would favor signals that are costly to the signaler and therefore are likely to convey reliable information because they cannot be easily faked. Toxins in low concentrations may commonly act as signals between plants rather than as inhibitory allelochemicals. This explains why toxic concentrations of plant allelochemicals are rarely found in natural coevolved systems.
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Herbivore attack is known to increase the emission of volatiles, which attract predators to herbivore-damaged plants in the laboratory and agricultural systems. We quantified volatile emissions fromNicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually. Three compounds (cis-3-hexen-1-ol, linalool, and cis-α-bergamotene) increased egg predation rates by a generalist predator; linalool and the complete blend decreased lepidopteran oviposition rates. As a consequence, a plant could reduce the number of herbivores by more than 90% by releasing volatiles. These results confirm that indirect defenses can operate in nature.
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Plants respond to insect herbivory by synthesizing and releasing complex blends of volatile compounds, which provide important host-location cues for insects that are natural enemies of herbivores. The effects of these volatile blends on herbivore behaviour have been investigated to only a limited extent, in part because of the assumption that herbivore-induced volatile emissions occur mainly during the light phase of the photoperiod. Because many moths-whose larvae are some of the most important insect herbivores-are nocturnal, herbivore-induced plant volatiles have not hitherto been considered to be temporally available as host-location cues for ovipositing females. Here we present chemical and behavioural assays showing that tobacco plants (Nicotiana tabacum) release herbivore-induced volatiles during both night and day. Moreover, several volatile compounds are released exclusively at night and are highly repellent to female moths (Heliothis virescens). The demonstration that tobacco plants release temporally different volatile blends and that lepidopteran herbivores use induced plant signals released during the dark phase to choose sites for oviposition adds a new dimension to our understanding of the role of chemical cues in mediating tritrophic interactions.
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Many plants invest carbon to form isoprene. The role of isoprene in plants is unclear, but many experiments showed that isoprene may have a role in protecting plants from thermal damage. A more general antioxidant action has been recently hypothesized on the basis of the protection offered by exogenous isoprene in nonemitting plants exposed to acute ozone doses. We inhibited the synthesis of endogenous isoprene by feeding fosmidomycin and observed that Phragmites australis leaves became more sensitive to ozone than those leaves forming isoprene. Photosynthesis, stomatal conductance, and fluorescence parameters were significantly affected by ozone only in leaves on which isoprene was not formed. The protective effect of isoprene was more evident when the leaves were exposed for a long time (8 h) to relatively low (100 nL L(-1)) ozone levels than when the exposure was short and acute (3 h at 300 nL L(-1)). Isoprene quenched the amount of H(2)O(2) formed in leaves and reduced lipid peroxidation of cellular membranes caused by ozone. These results indicate that isoprene may exert its protective action at the membrane level, although a similar effect could be obtained if isoprene reacted with ozone before forming active oxygen species. Irrespective of the mechanism, our results suggest that endogenous isoprene has an important antioxidant role in plants.
Code
R package for Data Analysis using multilevel/hierarchical model
Chapter
Red alder (Alnus rubra) and Sitka willow (Salix sitchensis) trees subjected to attack by tent caterpillars (Malacosoma californicum pluviale) or webworms (Hyphantria cunea), respectively, exhibited a change in foliage quality such that bioassay insects fed leaves from the attacked trees grew more slowly than those fed leaves from unattacked control trees. In contrast, bioassay of leaf quality of S. sitchensis, subjected to attack by tent caterpillars, indicated that altered leaf quality had been induced not only in the attacked trees but also in nearby unattacked control trees. This suggests that S. sitchensis is sensitive to and can respond to signals generated by attacked trees or the caterpillars. Since no evidence was found for root connections between attacked and control willows, the message may be transferred through airborne pheromonal substances.
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