RESUMEN

Plant resource allocation strategies are thought to be largely a consequence of changing abiotic conditions and evolutionary history. However, biotic interactions also influence how a plant allocates resources. As a result, plants mediate indirect interactions between organisms above- and belowground through resource allocation. Neighboring plants can influence plant fitness directly through competition for resources, and indirectly by altering associated community interactions (associational effects), such as pollination, herbivory, and a suite of belowground interactions. Given the importance of community interactions for plant success, and the known ability for plant neighbors to change these interactions, the goal of this "pandemic project" was to understand how heterospecific plant neighbors alter plant resource allocation, whether this occurred through above- or belowground mechanisms, and whether this in turn alters biotic interactions and the relationship between a focal plant and its herbivore and soil community interactions. To do so, we established a common garden experiment, manipulating plant neighbor identity and the extent of interaction among neighbors (aboveground only, vs. above- and belowground interactions, using customized pot types), and measured changes to a focal plant and its biotic interactions over two growing seasons. We found evidence of both neighbor effects and pot type, showing that neighbor interactions affect a focal plant through both above- and belowground processes, and how the focal plant is affected depends on neighbor identity. Though neighbors did not directly alter herbivory or most soil microbial interactions, they did alter the relationship between belowground microbial communities and a plant response trait (specific leaf area). Plant resource allocation responses were reduced with time, showing the importance of extending experiments beyond a single growing season, and are an important consideration when making predictions about plant responses to changing conditions. This study contributes to a growing body of work showing how community contexts affect the above- and belowground interactions of a plant through plant resource allocation strategies.

RESUMEN

Associational effects, whereby plants influence the biotic interactions of their neighbors, are an important component of plant-insect interactions. Plant chemistry has been hypothesized to mediate these interactions. The role of chemistry in associational effects, however, has been unclear in part because the diversity of plant chemistry makes it difficult to tease apart the importance and roles of particular classes of compounds. We examined the chemical ecology of associational effects using backcross-bred plants of the Solanum pennellii introgression lines. We used eight genotypes from the introgression line system to establish 14 unique neighborhood treatments that maximized differences in acyl sugars, proteinase inhibitor, and terpene chemical diversity. We found that the chemical traits of the neighboring plant, rather than simply the number of introgression lines within a neighborhood, influenced insect abundance on focal plants. Furthermore, within-chemical class diversity had contrasting effects on herbivore and predator abundances, and depended on the frequency of neighboring plant chemotypes. Notably, we found insect mobility-flying versus crawling-played a key role in insect response to phytochemistry. We highlight that the frequency and chemical phenotype of plant neighbors underlie associational effects and suggest this may be an important mechanism in maintaining intraspecific phytochemical variation within plant populations.

Asunto(s)

RESUMEN

Intercropping is drawing increasing attention as a strategy to increase crop yields and manage pest pressure, however the mechanisms of associational resistance in diversified cropping systems remain controversial. We conducted a controlled experiment to assess the impact of co-planting with silverleaf Desmodium (Desmodium uncinatum) on maize secondary metabolism and resistance to herbivory by the spotted stemborer (Chilo partellus). Maize plants were grown either in the same pot with a Desmodium plant or adjacent to it in a separate pot. Our findings indicate that co-planting with Desmodium influences maize secondary metabolism and herbivore resistance through both above and below-ground mechanisms. Maize growing in the same pot with a Desmodium neighbor was less attractive for oviposition by spotted stemborer adults. However, maize exposed only to above-ground Desmodium cues generally showed increased susceptibility to spotted stemborer herbivory (through both increased oviposition and larval consumption). VOC emissions and tissue secondary metabolite titers were also altered in maize plants exposed to Desmodium cues, with stronger effects being observed when maize and Desmodium shared the same pot. Specifically, benzoxazinoids were strongly suppressed in maize roots by direct contact with a Desmodium neighbor while headspace emissions of short-chain aldehydes and alkylbenzenes were increased. These results imply that direct root contact or soil-borne cues play an important role in mediating associational effects on plant resistance in this system.

Asunto(s)

RESUMEN

Spatial variation in plant community composition is an important driver of variation in susceptibility to herbivores. In close proximity, certain neighbors can attract or repel herbivores to a focal plant ("associational effects"). Neighboring plants may also compete for resources, modifying their phenotype in ways that affect susceptibility to herbivores. To test whether and how competition contributes to associational effects, we manipulated the sharing of belowground resources among plant neighbors (spotted Joe Pye weed and common boneset) that serve as alternate hosts for an herbivorous beetle. In the field, the beetle Ophraella notata laid more eggs and inflicted more damage on plants of both species that were released from belowground competition with neighbors. Competition also weakened the effects of neighbor identity during field trials, reducing associational susceptibility. When beetles were forced to choose between the two host species in cage trials, competition again reduced beetle use of Joe Pye weed as a secondary host. To test the role of plant traits related to herbivore defense and nutrition, we quantified leaf protein, specific leaf area, and trichomes, and conducted behavioral assays on leaf disks. Beetles did not distinguish between Joe Pye weed treatments at the leaf disk level, and competition did not impact specific leaf area and protein. Trichome density was higher in both species in the preferred treatment. Overall, our results suggest that belowground interactions between plants may mediate the strength of associational effects, as secondary hosts become more attractive when released from competition with primary host plants.

Asunto(s)

RESUMEN

Selective browsing by deer on young trees may impede the management goal of increasing forest resilience against climate change and other disturbances. Deer population density is often considered the main driver of browsing impacts on young trees, however, a range of other variables such as food availability also affect this relationship. In this study, we use browsing survey data from 135 research plots to explore patterns of roe deer (Capreolus capreolus) browsing pressure on woody plants in mountainous forests in central Europe. We fitted species-specific generalised linear mixed models for eight woody taxa, assessing the potential effects of understory characteristics, roe deer abundance and lying deadwood on browsing intensity. Our study reveals conspecific and associational effects for woody taxa that are intermediately browsed by roe deer. Selective browsing pressure was mediated by preferences of plants, in that, browsing of strongly preferred woody taxa as for example mountain ash (Sorbus aucuparia) and of least preferred woody taxa, for example Norway spruce (Picea abies) was not affected by the surrounding understory vegetation, while browsing pressure on intermediately browsed species like for example silver fir (Abies alba) was affected by understory characteristics. Contrary to our expectations, roe deer abundance was only positively associated with browsing pressure on silver fir and bilberry (Vaccinium myrtillus), while all other plants were unaffected by deer abundance. Finally, we did not find an influence of lying deadwood volume on the browsing pressure on any woody-plant species. Overall, our results indicate that patterns in browsing preference and intensity are species-specific processes and are partly affected by the surrounding understory vegetation. Current management strategies that aim to reduce browsing pressure through culling may be inefficient as they do not address other drivers of browsing pressure. However, managers also need to consider the characteristics of the local understory vegetation in addition to deer abundance and design species-specific plans to reduce browsing on woody plant taxa.

RESUMEN

It is commonly expected that exotic plants experience reduced herbivory, but experimental evidence for such enemy release is still controversial. One reason for conflicting results might be that community context has rarely been accounted for, although the surrounding plant diversity may moderate enemy release. Here, we tested the effects of focal tree origin and surrounding tree diversity on herbivore abundance and leaf damage in a cross-Atlantic tree-diversity experiment in Canada and Germany. We evaluated six European tree species paired with six North American congeners in both their native and exotic range, expecting lower herbivory for the exotic tree species in each pair at each site. Such reciprocal experiments have long been called for, but have not been realized thus far. In addition to a thorough evaluation of overall enemy release effects, we tested whether enemy release effects changed with the surrounding tree diversity. Herbivore abundance was indeed consistently lower on exotics across all six tree genera (12 comparisons). This effect of exotic status was independent of the continent, phylogenetic relatedness, and surrounding tree diversity. In contrast, leaf damage associated with generalist leaf chewers was consistently higher on North American tree species. Interestingly, several species of European weevils were the most abundant leaf chewers on both continents and the dominant herbivores at the Canadian site. Thus, most observed leaf damage is likely to reflect the effect of generalist herbivores that feed heavily on plant species with which they have not evolved. At the German site, sap suckers were the dominant herbivores and showed a pattern consistent with enemy release. Taken together, the consistently lower herbivory on exotics on both continents is not purely a pattern of enemy release in the strictest sense, but to some degree additionally reflects the susceptibility of native plants to invasive herbivores. In conclusion, our cross-Atlantic study is consistent with the idea that nonnative trees have generally reduced herbivory, regardless of tree community diversity and species identity, but for different reasons depending on the dominant herbivore guild.

Asunto(s)

RESUMEN

Leaf traits often vary with plant neighbourhood composition, which in turn may mediate plant susceptibility to herbivory. However, it is unknown whether there are any common patterns of change in leaf trait expression in response to neighbourhood diversity, and whether these responses confer increased resistance or susceptibility to herbivores.We used meta-analysis to combine data from 43 studies that examined the influence of neighbourhood diversity on eight physical and chemical leaf traits that could affect herbivory. All leaf traits apart from leaf thickness were highly plastic and exhibited significant differences between plant monocultures and species mixtures, but the direction of effect was variable. Leaf toughness was the only trait that displayed a significant decrease with plant diversity, whereas specific leaf area (SLA) and leaf nitrogen were both marginally increased in species mixtures.The magnitude and direction of leaf trait responses to neighbourhood diversity were independent of plant density and phylogenetic diversity, but changes in SLA correlated positively with plant species richness. SLA was also significantly increased in experimental studies, but not in observational studies, while neighbourhoods containing nitrogen-fixers were associated with increased leaf nitrogen and reduced phenolics. When studies on the over-represented species Betula pendula were removed from the analysis, the effect of neighbourhood diversity on leaf toughness became nonsignificant, but phenolics were significantly reduced in diverse neighbourhoods composed of mature trees, and marginally reduced in species mixtures across all studies.Increases in plant neighbourhood diversity are often associated with reductions of herbivory, although in some cases, the reverse occurs, and plants growing in species mixtures are found to suffer greater herbivory than those in monocultures. This study offers a potential explanation for the latter phenomenon, as our results show that leaf trait expression is highly plastic in response to neighbourhood diversity, and in certain cases could lead to increased leaf quality, which in turn could promote greater rates of herbivory. Read the free Plain Language Summary for this article on the Journal blog.

RESUMEN

Associational effects-in which the vulnerability of a plant to herbivores is influenced by its neighbors-have been widely implicated in mediating plant-herbivore interactions. Studies of associational effects typically focus on interspecific interactions or pest-crop dynamics. However, associational effects may also be important for species with intraspecific variation in defensive traits. In this study, we observed hundreds of Datura wrightii-which exhibits dimorphism in its trichome phenotype-from over 30 dimorphic populations across California. Our aim was to determine whether a relationship existed between the trichome phenotype of neighboring conspecifics and the likelihood of being damaged by four species of herbivorous insects. We visited plants at three timepoints to assess how these effects vary both within and between growing seasons. We hypothesized that the pattern of associational effects would provide rare morphs (i.e., focal plants that are a different morph than their neighbors) with an advantage in the form of reduced herbivory, thereby contributing to the negative frequency-dependent selection previously documented in this system. We found the best predictor of herbivory/herbivore presence on focal plants was the phenotype of the focal plant. However, we also found some important neighborhood effects. The total number of plants near a focal individual predicted the likelihood and/or magnitude of herbivory by Tupiochoris notatus, Lema daturaphila, and Manduca sexta. We also found that velvety focal plants with primarily sticky neighbors are more susceptible to infestation by Tupiochoris notatus and Lema daturaphila. This does not align with the hypothesis that associational effects at the near-neighbor scale contribute to a rare-morph advantage in this system. Overall, the results of our study show that the number and trichome-morph composition of neighboring conspecifics impact interactions between D. wrightii and insect herbivores.

RESUMEN

For some animals, the habitat which they first experience can influence the type of habitat which they select later in life and, thus, potentially their population distribution and dynamics. However, for many insect herbivores, whose natal habitat may consist of a single hostplant, the consequences of natal hostplant experience remain untested in landscapes relevant to the adult, which may select not only among plants, but among plant patches. As a first step towards understanding how natal hostplant experience shapes patterns of insect feeding damage in landscapes relevant to adults, we conducted partially caged field experiments with diamondback moths that were reared on either mustard or collard plants and then allowed to choose among and within patches of plants that varied in plant density and composition. We predicted that natal hostplant experience would interact with patch size and composition to influence the number of diamondback moth offspring and feeding damage per plant. As predicted, when moths were reared on collards, we found more offspring on and damage to collard plants in four-collard patches than in two-collard patches (i.e., resource concentration), but no difference when moths were reared on mustards. Contrary to predictions, we found no difference in the number of offspring on or damage to mixed plant patches compared with two- or four-collard plant patches regardless of natal hostplant type. Our research suggests that prior hostplant experience has complex consequences for how insects and their feeding damage are distributed in patchy environments and highlights the need for future research in this area.

Asunto(s)

RESUMEN

Many chemically defended aposematic species are characterized by relatively low toxin levels, which enables predators to include them in their diets under certain circumstances. Knowledge of the conditions governing the survival of such prey animals-especially in the context of the co-occurrence of similar but undefended prey, which may result in mimicry-like interactions-is crucial for understanding the initial evolution of aposematism. In a one-month outdoor experiment using fish (the common carp Cyprinus carpio) as predators, we examined the survival of moderately defended aposematic tadpole prey (the European common toad Bufo bufo) with varying absolute densities in single-species prey systems or varying relative densities in two-species prey systems containing morphologically similar but undefended prey (the European common frog Rana temporaria). The density effects were investigated in conjunction with the hunger levels of the predator, which were manipulated by means of the addition of alternative (nontadpole) food. The survival of the B. bufo tadpoles was promoted by increasing their absolute density in the single-species prey systems, increasing their relative density in the two-species prey systems, and providing ample alternative food for the predator. Hungry predators eliminated all R. temporaria individuals regardless of their proportion in the prey community; in treatments with ample alternative food, high relative B. bufo density supported R. temporaria survival. The results demonstrated that moderately defended prey did benefit from high population densities (both absolute and relative), even under long-term predation pressure. However, the physiological state of the predator was a crucial factor in the survival of moderately defended prey. While the availability of alternative prey in general should promote the spread and maintenance of aposematism, the results indicated that the resemblance between the co-occurring defended and undefended prey may impose mortality costs on the defended model species, even in the absence of actual mimicry.

RESUMEN

Volatile organic compounds (VOCs) emitted by plant leaves can influence the physiology of neighbouring plants. In contrast to leaf VOCs, little is known about the role of root VOCs in plant-plant interactions. Here, we characterize constitutive root VOC emissions of the spotted knapweed (Centaurea stoebe) and explore the impact of these VOCs on the germination and growth of different sympatric plant species. We show that C. stoebe roots emit high amounts of sesquiterpenes, with estimated release rates of (E)-ß-caryophyllene above 3 µg g-1  dw hr-1 . Sesquiterpene emissions show little variation between different C. stoebe populations but vary substantially between different Centaurea species. Through root transcriptome sequencing, we identify six root-expressed sesquiterpene synthases (TPSs). Two root-specific TPSs, CsTPS4 and CsTPS5, are sufficient to produce the full blend of emitted root sesquiterpenes. VOC-exposure experiments demonstrate that C. stoebe root VOCs have neutral to positive effects on the germination and growth of different sympatric neighbours. Thus, constitutive root sesquiterpenes produced by two C. stoebe TPSs are associated with facilitation of sympatric neighbouring plants. The release of root VOCs may thus influence plant community structure in nature.

Asunto(s)

RESUMEN

Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighbouring plants. However, little is known about the effects of root VOCs on plant-herbivore interactions of neighbouring plants. The spotted knapweed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on the primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant-mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C.stoebe root VOCs does not affect the accumulation of defensive secondary metabolites but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)-ß-caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant-herbivore interactions of neighbouring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.

Asunto(s)

RESUMEN

Many insect species have limited sensory abilities and may not be able to perceive the quality of different resource types while approaching patchily distributed resources. These restrictions may lead to differences in selection rates between separate patches and between different resource types within a patch, which may have consequences for associational effects between resources. In this study, we used an oviposition assay containing different frequencies of apple and banana substrates divided over two patches to compare resource selection rates of wild-type Drosophila melanogaster at the between- and within-patch scales. Next, we compared the wild-type behavior with that of the olfactory-deficient strain Orco 2 and the gustatory-deficient strain Poxn ΔM22-B5 and found comparable responses to patch heterogeneity and similarly strong selection rates for apple at both scales for the wild-type and olfactory-deficient flies. Their oviposition behavior translated into associational susceptibility for apple and associational resistance for banana. The gustatory-deficient flies, on the other hand, no longer had a strong selection rate for apple, strongly differed in between- and within-patch selection rates from the wild-type flies, and caused no associational effects between the resources. Our study suggests that differences in sensory capabilities can affect resource selection at different search behavior scales in different ways and in turn underlie associational effects between resources at different spatial scales.

RESUMEN

Despite our understanding of chemical defenses and their consequences for plant performance and herbivores, we know little about whether defensive chemicals in plant tissues, such as alkaloids, and their spatial variation within a population play unappreciated and critical roles in plant-herbivore interactions. Neighboring plants can decrease or increase attractiveness of a plant to herbivores, an example of a neighborhood effect. Chemical defensive traits may contribute to neighborhood effects in plant-herbivore interactions. We examined the effects of nicotine in leaves (a non-emitted defense chemical) on plant-herbivore interactions in a spatial context, using two varieties of Nicotiana tabacum with different nicotine levels. A common garden experiment demonstrated that visits by grasshoppers decreased with increasing density of neighboring plants with a greater nicotine level. In contrast, visits of leaf caterpillars were not affected by neighbors, irrespective of nicotine levels. Thus, our results clearly highlighted that the neighborhood effect caused by the nicotine in leaves depended on the insect identity, and it was mediated by plant-herbivore interactions, rather than plant-plant interactions. This study demonstrates that understanding of effects of plant defensive traits on plant-herbivore interactions requires careful consideration of the spatial distribution of plant defenses, and provides support for the importance of spatial context to accurately capture the ecological and evolutionary consequences of plant-herbivore interactions.

RESUMEN

The diversity of plant neighbors commonly results in direct, bottom-up effects on herbivore ability to locate their host, and in indirect effects on herbivores involving changes in plant traits and a top-down control by their enemies. Yet, the relative contribution of bottom-up and top-down forces remains poorly understood. We also lack knowledge on the effect of abiotic constraints such as summer drought on the strength and direction of these effects. We measured leaf damage on pedunculate oak (Quercus robur), alone or associated with birch, pine or both in a long-term tree diversity experiment (ORPHEE), where half of the plots were irrigated while the other half remained without irrigation and received only rainfall. We tested three mechanisms likely to explain the effects of oak neighbors on herbivory: (1) Direct bottom-up effects of heterospecific neighbors on oak accessibility to herbivores, (2) indirect bottom-up effects of neighbors on the expression of leaf traits, and (3) top-down control of herbivores by predators. Insect herbivory increased during the growth season but was independent of neighbor identity and irrigation. Specific leaf area, leaf toughness, and thickness varied with neighbor identity while leaf dry matter content or C:N ratio did not. When summarized in a principal component analysis (PCA), neighbor identity explained 87% of variability in leaf traits. PCA axes partially predicted herbivory. Despite greater rates of attack on dummy caterpillars in irrigated plots, avian predation, and insect herbivory remained unrelated. Our study suggests that neighbor identity can indirectly influence insect herbivory in mixed forests by modifying leaf traits. However, we found only partial evidence for these trait-mediated effects and suggest that more attention should be paid to some unmeasured plant traits such as secondary metabolites, including volatile organic compounds, to better anticipate the effects of climate change on plant-insect interactions in the future.

RESUMEN

Movement of individuals links the effects of local variation in habitat quality with growth and persistence of populations at the landscape scale. When the populations themselves are linked by interspecific interactions, such as predation, differential movement between habitats may lead to counterintuitive system-wide dynamics. Understanding the interaction between local drivers and dynamics of widely dispersed species is necessary to predict the impacts of habitat fragmentation and degradation, which may be transmitted across habitat boundaries by species' movements. Here we model predator-prey interactions across unaltered and degraded habitat areas, and we explore the additional effects of adaptive habitat choice by predators on the resilience of prey populations. We show how movement between habitats can produce the "bad neighbor effect," in which predators' response to localized habitat degradation causes system-wide loss of prey populations. This effect arises because adaptive foraging results in the concentration of predators in the more productive unaltered habitat, even when this habitat can not support the increased prey mortality. The mechanisms underlying this effect are especially sensitive to prey dispersal rate and adaptive predator behavior.

Asunto(s)

RESUMEN

Despite increasing evidence that herbivory on a focal plant may hinge upon the identity of its neighbors, it is not clear whether predictable mechanisms govern the nature and magnitude of such associational effects. Using a factorial field experiment replicated at 14 sites across 80,000 hectares, we evaluated the mechanisms driving associational effects between two plant species mediated by grasshopper herbivores. Our experiment manipulated local neighborhood plant density (two levels) and frequency (three levels), nested within two larger-scale habitat contexts (habitats that did or did not have past agricultural land use). We found that the more palatable plant species, Solidago nemoralis, experienced reduced herbivory (associational resistance) when rare due mainly to reduced grasshopper foraging activity. Damage to the less palatable plant species, S. odora, was affected by the interaction between plant frequency and the land-use history of the site: it experienced increased damage (associational susceptibility) in even-frequency neighborhoods, but only in sites with a history of agricultural use. Behavioral assays generally corroborated the results from the field, further supporting the importance of foraging behavior in generating associational effects. In finding that associational effects are contingent upon relative palatability among plants and events in the distant past that modify contemporary habitat structure (i.e., past agricultural land use), our work suggests that foraging decisions made at the neighborhood level are important for generating associational effects and that in some cases these neighborhood interactions also depend on the larger-scale environmental context resulting from legacies of past land-use events.

Asunto(s)

RESUMEN

The presence of nonprey or nonhosts is known to reduce the strength of consumer- resource interactions by increasing the consumer's effort needed to find its resource. These interference effects can have a stabilizing effect on consumer-resource dynamics, but have also been invoked to explain parasitoid extinctions. To understand how nonhosts affect parasitoids, we manipulated the density and diversity of nonhost aphids using experimental host-parasitoid communities and tested how this affects parasitation efficiency of two aphid parasitoid species. To further study the behavioral response of parasitoids to nonhosts, we tested for changes in parasitoid time allocation in relation to their host-finding strategies. The proportion of successful attacks (attack rate) in both parasitoid species was reduced by the presence of nonhosts. The parasitoid Aphidius megourae was strongly affected by increasing nonhost diversity with the attack rate dropping from 0.39 without nonhosts to 0.05 with high diversity of nonhosts, while Lysiphlebus fabarum responded less strongly, but in a more pronounced way to an increase in nonhost density. Our experiments further showed that increasing nonhost diversity caused host searching and attacking activity levels to fall in A. megourae, but not in L. fabarum, and that A. megourae changed its behavior after a period of time in the presence of nonhosts by increasing its time spent resting. This study shows that nonhost density and diversity in the environment are crucial determinants for the strength of consumer-resource interactions. Their impact upon a consumer's efficiency strongly depends on its host/prey finding strategy as demonstrated by the different responses for the two parasitoid species. We discuss that these trait-mediated indirect interactions between host and nonhost species are important for community stability, acting either stabilizing or destabilizing depending on the level of nonhost density or diversity present.