Seasonality of herbivory and communication between individuals of sagebrush

Seasonal changes in herbivore numbers and in plant defenses are well known to influence plant–herbivore interactions. Some plant defenses are induced in response to herbivore attack or cues correlated with risk of attack although seasonal variation in these defenses is relatively poorly known. We previously reported that sagebrush becomes more resistant to its herbivores when neighboring plants have been experimentally clipped with scissors. In this study we asked whether herbivory to leaves of sagebrush varied seasonally and whether there was seasonal variation in natural levels of damage when neighbors were clipped. We found that sagebrush accumulated most chewing damage early in the season, soon after the spring flush of new leaves. This damage was caused by generalist grasshoppers, deer, specialist caterpillars, beetles, gall makers, and other less common herbivores. Sagebrush showed no evidence of preferentially abscising leaves that had been experimentally clipped. Experimental clipping by Trirhabda pilosa beetle larvae caused neighbors to accumulate less herbivore damage later that season, similar to results in which clipping was done with scissors. Induced resistance caused by experimentally clipping a neighbor was affected by season; plants with neighbors clipped in May accumulated less damage throughout the season relative to plants with unclipped neighbors or neighbors clipped later in the summer. We found a correlation between seasonal herbivore pressure, damage accumulated by plants, and induced responses to experimentally clipping neighbors. The causal mechanisms responsible for this correlation are unknown although a strong seasonal effect was clear.     

Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants

Whether plants respond to cues produced by neighbors has been a topic of much debate. Recent evidence suggests that wild tobacco plants transplanted near experimentally clipped sagebrush neighbors suffer less leaf herbivory than tobacco controls with unclipped neighbors. Here we expand these results by showing evidence for induced resistance in naturally rooted tobacco when sagebrush neighbors are clipped either with scissors or damaged with actual herbivores. Tobacco plants with sagebrush neighbors clipped in both ways had enhanced activity levels of polyphenol oxidase (PPO), a chemical marker of induced resistance in many solanaceous plants. Eavesdropping was found for plants that were naturally rooted, although only when sagebrush and tobacco grew within 10 cm of each other. Although tobacco with clipped neighbors experienced reduced herbivory, tobacco that grew close to sagebrush had lower production of capsules than plants that grew far from sagebrush. When neighboring tobacco rather than sagebrush was clipped, neither levels of PPO nor levels of leaf damage to tobacco were affected. Eavesdropping on neighboring sagebrush, but not neighboring tobacco, may result from plants using a jasmonate signaling system. These results indicate that plants eavesdrop in nature and that this behavior can increase resistance to herbivory although it does not necessarily increase plant fitness.     

Prolonged exposure is required for communication in sagebrush

Volatile communication allows plants to coordinate systemic induced resistance against herbivores. The mechanisms responsible and nature of the cues remain poorly understood. It is unknown how plants distinguish between reliable cues and misinformation. Previous experiments in which clipped sagebrush branches were bagged suggested that cues are emitted or remain active for up to 3 days. We conducted experiments using plastic bags to block emission of cues at various times following experimental clipping. We also collected headspace volatiles from clipped and unclipped branches for 1 h, transferred those volatiles to assay branches, and incubated the assays for either 1 or 6 h. We found that assay branches that received volatile cues for less than 1 h following clipping of neighbors failed to induce resistance. Assay branches that received volatile cues for more than 1 h experienced reduced herbivory throughout the season. Branches incubated for 6 h with volatiles that had been collected during the first hour following clipping showed induced resistance. These results indicate that sagebrush must receive cues for an extended time (>1 h) before responding; they suggest that the duration of cue reception is an important and overlooked process in communication allowing plants to avoid unreliable, ephemeral cues.     

Induced Resistance in Wild Tobacco with Clipped Sagebrush Neighbors: The Role of Herbivore Behavior

Previous experiments showed that wild tobacco plants with experimentally clipped sagebrush neighbors experienced less damage by grasshoppers than tobacco plants with unclipped sagebrush neighbors. This result could have been caused by grasshoppers preferring not to feed near clipped sagebrush. This hypothesis was tested in field choice experiments using six grasshopper species feeding on an unresponsive and uniformly palatable food. When offered food that was either close to clipped sagebrush or close to unclipped sagebrush, grasshoppers showed no preference. When offered food that was either close to sagebrush (3 cm) or far from sagebrush (30 cm), grasshoppers preferred to feed far from sagebrush. However, this preference was similar whether or not the sagebrush had been clipped. Avoidance of feeding near clipped sagebrush, independent of changes in tobacco, was not found to contribute to our earlier result that tobacco near clipped sagebrush suffered less herbivory than tobacco near unclipped sagebrush.     

Communication between sagebrush and wild tobacco in the field

Communication between plants has not been widely accepted by most ecologists. However, recent field experiments indicated that wild tobacco plants became more resistant to herbivores when grown in close proximity to clipped sagebrush neighbors. Tobacco plants grown within 15 cm of sagebrush that had been either manually clipped with scissors or damaged by herbivores experienced less naturally occurring folivory than tobacco plants with unclipped neighbors. These results were consistent over five field seasons and involved treatments that were randomly assigned and well replicated. Associated with lower levels of herbivory were increased activities of polyphenol oxidase in tobacco foliage near clipped sagebrush neighbors. Experiments that blocked either air or soil contact between sagebrush and tobacco indicated that the communication was airborne rather than soilborne. Alternative explanations involving altered microenvironmental conditions or avoidance of clipped sagebrush by herbivores were not supported.Much remains to be learned about the natural history of this phenomenon. Apparently the plants must be in close proximity for communication to occur. Preliminary results suggest that communication between sagebrush and other plants may also occur. The mechanisms of communication as well as its ecological and evolutionary significance remain unknown.     

Specific herbivore-induced volatiles defend plants and determine insect community composition in the field

In response to insect attack, plants release complex blends of volatile compounds. These volatiles serve as foraging cues for herbivores, predators and parasitoids, leading to plant-mediated interactions within and between trophic levels. Hence, plant volatiles may be important determinants of insect community composition. To test this, we created rice lines that are impaired in the emission of two major signals, S-linalool and (E)-β-caryophyllene. We found that inducible S-linalool attracted predators and parasitoids as well as chewing herbivores, but repelled the rice brown planthopper Nilaparvata lugens, a major pest. The constitutively produced (E)-β-caryophyllene on the other hand attracted both parasitoids and planthoppers, resulting in an increased herbivore load. Thus, silencing either signal resulted in specific insect assemblages in the field, highlighting the importance of plant volatiles in determining insect community structures. Moreover, the results imply that the manipulation of volatile emissions in crops has great potential for the control of pest populations.     

Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context

Herbivorous and carnivorous arthropods use plant volatiles when foraging for food. In response to herbivory, plants emit a blend that may be quantitatively and qualitatively different from the blend emitted when intact. This induced volatile blend alters the interactions of the plant with its environment. We review recent developments regarding the induction mechanism as well as the ecological consequences in a multitrophic and evolutionary context. It has been well established that carnivores (predators and parasitoids) are attracted by the volatiles induced by their herbivorous victims. This concerns an active plant response. In the case of attraction of predators, this is likely to result in a fitness benefit to the plant, because through consumption a predator removes the herbivores from the plant. However, the benefit to the plant is less clear when parasitoids are attracted, because parasitisation does usually not result in an instantaneous or in a complete termination of consumption by the herbivore. Recently, empirical evidence has been obtained that shows that the plant's response can increase plant fitness, in terms of seed production, due to a reduced consumption rate of parasitized herbivores. However, apart from a benefit from attracting carnivores, the induced volatiles can have a serious cost because there is an increasing number of studies that show that herbivores can be attracted. However, this does not necessarily result in settlement of the herbivores on the emitting plant. The presence of cues from herbivores and/or carnivores that indicate that the plant is a competitor- and/or enemy-dense space, may lead to an avoidance response. Thus, the benefit of emission of induced volatiles is likely to depend on the prevailing faunal composition. Whether plants can adjust their response and influence the emission of the induced volatiles, taking the prevalent environmental conditions into account, is an interesting question that needs to be addressed. The induced volatiles may also affect interactions of the emitting plant with its neighbours, e.g., through altered competitive ability or by the neighbour exploiting the emitted information.Major questions to be addressed in this research field comprise mechanistic aspects, such as the identification of the minimally effective blend of volatiles that explains the attraction of carnivores to herbivore-infested plants, and evolutionary aspects such as the fitness consequences of induced volatiles. The elucidation of mechanistic aspects is important for addressing ecological and evolutionary questions. For instance, an important tool to address ecological and evolutionary aspects would be to have plant pairs that differ in only a single trait. Such plants are likely to become available in the near future as a result of mechanistic studies on signal-transduction pathways and an increased interest in molecular genetics.     

Leaf compensatory growth as a tolerance strategy to resist herbivory in Pancratium sickenbergeri

We examined the effects of leaf herbivory by the dorcas gazelle, Gazella dorcas, on the compensatory growth of the geophyte Pancratium sickenbergeri (Amaryllidaceae) in the Negev desert, Israel. In three populations exposed to different levels of herbivory, we removed different amounts of photosynthetic leaf area from plants in five clipping treatments: 0, 25, 50%-dispersed over all leaves, 50%-entire area of half the leaves, 100%. The population with the lowest level of herbivory showed the lowest relative regrowth rate after clipping. In the population with a constantly high level of herbivory, plants in intermediate-clipping treatments overcompensated in leaf area after clipping. For all the populations, clipped plants produce more new leaves than unclipped plants. In the population with the highest level of herbivory, clipping treatments did not have a significant effect on the number of fruits per plant. In addition, we did not find a trade-off between investments in growth and reproduction in this population. Our results indicated that, in the desert lily, herbivores may select for plant mechanisms that compensate after damage as a tolerant strategy to maintain fitness.     

Experimental clipping of sagebrush inhibits seed germination of neighbours

Current views of plant communities emphasize the importance of competition for resources and colonization ability in determining seedling establishment and plant distributions. Many desert shrubs are surrounded by bare zones that lack other plants or have different suites of species beneath them compared with the open desert surrounding them. Releases of biochemicals as volatiles from leaves, leachates from litter, or exudates from roots have been proposed as mechanisms for this pattern, but such phytotoxicity has been controversial. I tested the hypothesis that experimental clipping of sagebrush foliage enhances its effect as a germination inhibitor. Germination of native forbs and grasses was reduced in association with clipped, compared with unclipped, sagebrush foliage in lath house and field experiments. Sagebrush seeds were not significantly affected. Air contact was required for this inhibition of germination. Soil contact and leaf litter were not required and added little inhibition of germination. These results suggest a potentially large, indirect, and previously overlooked role for interactions between herbivory and germination that could affect plant community structure.     

When resources don't rescue: flowering phenology and species interactions affect compensation to herbivory in Ipomopsis aggregata

The ability of plants to tolerate, or compensate for, herbivore damage is highly variable and has been the subject of much research. Although many plants can compensate for herbivore damage, and some even overcompensate, we cannot yet generalize about the conditions that promote a positive response to damage. Here, we asked how abiotic resources (i.e. plant nutrient status) coupled with biotic interactions – i.e. subsequent interactions with pollinators, seed predators and nectar robbing bumble bees – affect the compensatory ability of Ipomopsis aggregata, a monocarpic herb that has been the subject of much previous debate. We hypothesized that compensation to herbivore damage in I. aggregata (Polemoniaceae) would depend first on plants having an ample supply of resources and, second, on the outcome of subsequent interactions with mutualist pollinators and enemy pre‐dispersal seed predators and nectar robbing bumble bees. We used a fully‐factorial experiment in which plants were watered, fertilized or left as unmanipulated controls, crossed with clipping to simulate herbivore damage to the apical meristem. Resource addition enhanced both male and female components of fitness, but resource enhancement did not provide the means for plants to fully compensate for simulated herbivory. Clipped plants produced significantly more inflorescences, but at the expense of a delay in flowering and fewer total flowers. Clipping significantly reduced losses to dipteran pre‐dispersal seed predators by delaying flowering time, but early flowering plants produced higher numbers of seeds despite incurring higher rates of predation. Clipped plants incurred a higher risk to nectar robbers in one of two years. Overall, clipped plants suffered severe reductions (a nearly 50% reduction in total seed set) in female success, but clipping combined with nutrient addition enhanced male function through increases in per‐flower pollen production. However, because clipped plants produced significantly fewer flowers than unclipped plants, whole‐plant pollen production was significantly reduced by clipping. Pollinator visitation and nectar robbing were variable between clipping treatments and between years and (nectar robbing) among sites. Our results demonstrate that the variability in plant response to herbivory can, at least in part, be driven by plant interactions with mutualists and enemies. Thus, accounting for such interactions and their variability is important to fully understanding plant compensation for herbivore damage and will likely go far to explain variation in plant response that appears to be independent of resources.     

Drought and Root Herbivory Interact to Alter the Response of Above-Ground Parasitoids to Aphid Infested Plants and Associated Plant Volatile Signals

Multitrophic interactions are likely to be altered by climate change but there is little empirical evidence relating the responses of herbivores and parasitoids to abiotic factors. Here we investigated the effects of drought on an above/below-ground system comprising a generalist and a specialist aphid species (foliar herbivores), their parasitoids, and a dipteran species (root herbivore).We tested the hypotheses that: (1) high levels of drought stress and below-ground herbivory interact to reduce the performance of parasitoids developing in aphids; (2) drought stress and root herbivory change the profile of volatile organic chemicals (VOCs) emitted by the host plant; (3) parasitoids avoid ovipositing in aphids feeding on plants under drought stress and root herbivory. We examined the effect of drought, with and without root herbivory, on the olfactory response of parasitoids (preference), plant volatile emissions, parasitism success (performance), and the effect of drought on root herbivory. Under drought, percentage parasitism of aphids was reduced by about 40–55% compared with well watered plants. There was a significant interaction between drought and root herbivory on the efficacy of the two parasitoid species, drought stress partially reversing the negative effect of root herbivory on percent parasitism. In the absence of drought, root herbivory significantly reduced the performance (e.g. fecundity) of both parasitoid species developing in foliar herbivores. Plant emissions of VOCs were reduced by drought and root herbivores, and in olfactometer experiments parasitoids preferred the odour from well-watered plants compared with other treatments. The present work demonstrates that drought stress can change the outcome of interactions between herbivores feeding above- and below-ground and their parasitoids, mediated by changes in the chemical signals from plants to parasitoids. This provides a new insight into how the structure of terrestrial communities may be affected by drought.     

Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush

The possibility of communication between plants was proposed nearly 20 years ago, although previous demonstrations have suffered from methodological problems and have not been widely accepted. Here we report the first rigorous, experimental evidence demonstrating that undamaged plants respond to cues released by neighbors to induce higher levels of resistance against herbivores in nature. Sagebrush plants that were clipped in the field released a pulse of an epimer of methyl jasmonate that has been shown to be a volatile signal capable of inducing resistance in wild tobacco. Wild tobacco plants with clipped sagebrush neighbors had increased levels of the putative defensive oxidative enzyme, polyphenol oxidase, relative to control tobacco plants with unclipped sagebrush neighbors. Tobacco plants near clipped sagebrush experienced greatly reduced levels of leaf damage by grasshoppers and cutworms during three field seasons compared to unclipped controls. This result was not caused by an altered light regime experienced by tobacco near clipped neighbors. Barriers to soil contact between tobacco and sagebrush did not reduce the difference in leaf damage although barriers that blocked air contact negated the effect. Received: 15 February 2000 / Accepted: 1 April 2000     

Seasonal variation of responses to herbivory and volatile communication in sagebrush (<Emphasis Type="Italic">Artemisia tridentata</Emphasis>) (Asteraceae)

Plants can respond to insect herbivory in various ways to avoid reductions in fitness. However, the effect of herbivory on plant performance can vary depending on the seasonal timing of herbivory. We investigated the effects of the seasonal timing of herbivory on the performance of sagebrush (Artemisia tridentata). Sagebrush is known to induce systemic resistance by receiving volatiles emitted from clipped leaves of the same or neighboring plants, which is called volatile communication. Resistance to leaf herbivory is known to be induced most effectively after volatile communication in spring. We experimentally clipped 25 % of leaves of sagebrush in May when leaves were expanding, or in July when inflorescences were forming. We measured the growth and flower production of clipped plants and neighboring plants which were exposed to volatiles emitted from clipped plants. The treatment conducted in spring reduced the growth of clipped plants. This suggests that early season leaf herbivory is detrimental because it reduces the opportunities for resource acquisition after herbivory, resulting in strong induction of resistance in leaves. On the other hand, the late season treatment increased flower production in plants exposed to volatiles, which was caused mainly by the increase in the number of inflorescences. Because the late season treatment occurred when sagebrush produces inflorescences, sagebrush may respond to late herbivory by increasing compensation ability and/or resistance in inflorescences rather than in leaves. Our results suggest that sagebrush can change responses to herbivory and subsequent volatile communication seasonally and that the seasonal variation in responses may reduce the cost of induced resistance.     

Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory

Plants infested with a single herbivore species can attract natural enemies through the emission of herbivore‐induced plant volatiles (HIPVs). However, under natural conditions plants are often attacked by more than one herbivore species. We investigated the olfactory response of a generalist predators Macrolophus caliginosus to pepper infested with two‐spotted spider mites, Tetranychus urticae, or green peach aphid, Myzus persicae, vs. plants infested with both herbivore species in a Y‐tube olfactometer set up. In addition, the constituents of volatile blends from plants exposed to multiple or single herbivory were identified by gas chromatography‐mass spectrometry (GC‐MS). The mirid bugs showed a stronger response to volatiles emitted from plants simultaneously infested with spider mites and aphids than to those emitted from plants infested by just one herbivore, irrespective of the species. Combined with results from previous studies under similar conditions we infer that this was a reaction to herbivore induced plant volatiles. The GC‐MS analysis showed that single herbivory induced the release of 22 additional compounds as compared with the volatiles emitted from clean plants. Quantitative analyses revealed that the amount of volatile blends emitted from pepper infested by both herbivores was significantly higher than that from pepper infested by a single herbivore. Moreover, two unique substances were tentatively identified (with a probability of 94% and 91%, respectively) in volatiles emitted by multiple herbivory damaged plants: α‐zingiberene and dodecyl acetate.     

Herbivory by a Phloem-feeding insect inhibits floral volatile production

There is extensive knowledge on the effects of insect herbivory on volatile emission from vegetative tissue, but little is known about its impact on floral volatiles. We show that herbivory by phloem-feeding aphids inhibits floral volatile emission in white mustard Sinapis alba measured by gas chromatographic analysis of headspace volatiles. The effect of the Brassica specialist aphid Lipaphis erysimi was stronger than the generalist aphid Myzus persicae and feeding by chewing larvae of the moth Plutella xylostella caused no reduction in floral volatile emission. Field observations showed no effect of L. erysimi-mediated floral volatile emission on the total number of flower visits by pollinators. Olfactory bioassays suggested that although two aphid natural enemies could detect aphid inhibition of floral volatiles, their olfactory orientation to infested plants was not disrupted. This is the first demonstration that phloem-feeding herbivory can affect floral volatile emission, and that the outcome of interaction between herbivory and floral chemistry may differ depending on the herbivore's feeding mode and degree of specialisation. The findings provide new insights into interactions between insect herbivores and plant chemistry.     

Effective distance of volatile cues for plant–plant communication in beech

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.     

Host plant scents attract rolled-leaf beetles to Neotropical gingers in a Central American tropical rain forest

Leaf volatile chemicals are known to reduce herbivory rates by repelling or intoxicating insect herbivores and by attracting the predators and parasitoids of herbivores. However, leaf volatiles may also be used by insect herbivores as cues to locate their host plants. Leaf volatiles are suggested to be important host search cues for herbivores in structurally complex and diverse habitats, such as tropical rain forests. A group of insect herbivores, the rolled-leaf beetles (Coleoptera: Chrysomelidae: Hispinae), have maintained a highly specialized interaction with Neotropical gingers (Zingiberales) for ca. 60 million years. In this study, we explored chemical attraction to host plants under controlled laboratory conditions, using four sympatric rolled-leaf beetle species, Cephaloleia dorsalis Baly, Cephaloleia erichsonii Baly, Cephaloleia fenestrata Weise, and Cephaloleia placida Baly. For each beetle species, we investigated (i) whether it was repelled or attracted by leaf scents produced by four host and four non-host plant species, including Neotropical gingers in the families Marantaceae, Costaceae, and Zingiberaceae; and (ii) its ability to use scents to detect its host plant. We found that rolled-leaf beetles can detect and are attracted by leaf volatiles from both host and non-host gingers. Additionally, when beetles were simultaneously exposed to leaf volatiles from host and non-host plants, three rolled-leaf beetle species were significantly more attracted by volatiles from their host plants than from non-hosts. Only one of the beetle species was not able to discriminate between host and non-host scents.     

Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize

Plant volatiles function as important signals for herbivores, parasitoids, predators, and neighboring plants. Herbivore attack can dramatically increase plant volatile emissions in many species. However, plants do not only react to herbivore-inflicted damage, but also already start adjusting their metabolism upon egg deposition by insects. Several studies have found evidence that egg deposition itself can induce the release of volatiles, but little is known about the effects of oviposition on the volatiles released in response to subsequent herbivory. To study this we measured the effect of oviposition by Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) moths on constitutive and herbivore-induced volatiles in maize (Zea mays L.). Results demonstrate that egg deposition reduces the constitutive emission of volatiles and suppresses the typical burst of inducible volatiles following mechanical damage and application of caterpillar regurgitant, a treatment that mimics herbivory. We discuss the possible mechanisms responsible for reducing the plant’s signaling capacity triggered by S. frugiperda oviposition and how suppression of volatile organic compounds can influence the interaction between the plant, the herbivore, and other organisms in its environment. Future studies should consider oviposition as a potential modulator of plant responses to insect herbivores.     

Insect herbivores as potential causes of mortality and adaptation in gallforming insects

Summary Recent studies have suggested that plant galls benefit only the insects living in them and not the host plants, and that galls are induced by insects primarily to improve the plant as a microenvironment or a food source. The potential advantage to insects of protection from their predators and parasitoids has been considered unclear and perhaps minor in importance. However, the potential threat to gallforming insects from other insect herbivores has usually been relatively neglected. This paper notes literature and observations which suggest that herbivores may either consume or be deterred by galls. Even soft leaf galls produced by Hormaphis and Phylloxera aphids appeared to deter some herbivores in the field. The threat of herbivory to galls might help explain general patterns of gall ecology and morphology, and deserves closer attention.