Tree diversity enhances predation by birds but not by arthropods across climate gradients.

Tree diversity can promote both predator abundance and diversity. However, whether this translates into increased predation and top-down control of herbivores across predator taxonomic groups and contrasting environmental conditions remains unresolved. We used a global network of tree diversity experiments (TreeDivNet) spread across three continents and three biomes to test the effects of tree species richness on predation across varying climatic conditions of temperature and precipitation. We recorded bird and arthropod predation attempts on plasticine caterpillars in monocultures and tree species mixtures. Both tree species richness and temperature increased predation by birds but not by arthropods. Furthermore, the effects of tree species richness on predation were consistent across the studied climatic gradient. Our findings provide evidence that tree diversity strengthens top-down control of insect herbivores by birds, underscoring the need to implement conservation strategies that safeguard tree diversity to sustain ecosystem services provided by natural enemies in forests.

Temporal variation in tree diversity effects on birds and its implications for top-down control of insect herbivores in a tropical system.

Tree diversity promotes predator abundance and diversity, but evidence linking these effects to increased predation pressure on herbivores remains limited. In addition, tree diversity effects on predators can vary temporally as a function of environmental variation, or due to contrasting responses by different predator types. In a multi-year study, we assessed temporal variation in tree diversity effects on bird community abundance, diversity, and predation rates as a whole and by functional group based on feeding guild (omnivores vs. insectivores) and migratory status (migrant vs. resident). To this end, we conducted bird point counts in tree monocultures and polycultures and assessed attacks on clay caterpillars four times over a 2-year period in a tree diversity experiment in Yucatan, Mexico. Tree diversity effects on the bird community varied across surveys, with positive effects on bird abundance and diversity in most but not all surveys. Tree diversity had stronger and more consistent effects on omnivorous and resident birds than on insectivorous and migratory species. Tree diversity effects on attack rates also varied temporally but patterns did not align with variation in bird abundance or diversity. Thus, while we found support for predicted increases in bird abundance, diversity, and predation pressure with tree diversity, these responses exhibited substantial variation over time and the former two were uncoupled from patterns of predation pressure, as well as contingent on bird functional traits. These results underscore the need for long-term studies measuring responses by different predator functional groups to better understand tree diversity effects on top-down control.

Consequences of arthropod community structure for an at-risk insectivorous bird.

Global declines in bird and arthropod abundance highlights the importance of understanding the role of food limitation and arthropod community composition for the performance of insectivorous birds. In this study, we link data on nestling diet, arthropod availability and nesting performance for the Coastal Cactus Wren (Campylorhynchus brunneicapillus sandiegensis), an at-risk insectivorous bird native to coastal southern California and Baja Mexico. We used DNA metabarcoding to characterize nestling diets and monitored 8 bird territories over two years to assess the relationship between arthropod and vegetation community composition and bird reproductive success. We document a discordance between consumed prey and arthropod biomass within nesting territories, in which Diptera and Lepidoptera were the most frequently consumed prey taxa but were relatively rare in the environment. In contrast other Orders (e.g., Hemiptera, Hymenoptera)were abundant in the environment but were absent from nestling diets. Accordingly, variation in bird reproductive success among territories was positively related to the relative abundance of Lepidoptera (but not Diptera), which were most abundant on 2 shrub species (Eriogonum fasciculatum, Sambucus nigra) of the 9 habitat elements characterized (8 dominant plant species and bare ground). Bird reproductive success was in turn negatively related to two invasive arthropods whose abundance was not associated with preferred bird prey, but instead possibly acted through harassment (Linepithema humile; Argentine ants) and parasite transmission or low nutritional quality (Armadillidium vulgare; "pill-bug"). These results demonstrate how multiple aspects of arthropod community structure can influence bird performance through complementary mechanisms, and the importance of managing for arthropods in bird conservation efforts.

The role of timing in intraspecific trait ecology.

Intraspecific trait variation has tremendous importance for species interactions and community composition. A major source of intraspecific trait variation is an organism's developmental stage; however, timing is rarely considered in studies of the ecological effects of intraspecific variation. Here, we examine the role of time in the ecology of intraspecific trait variation, focusing on plants and their interactions with other organisms. Trait variation due to differences in developmental timing has unique features and dynamics, distinguishing it from variation due to genes or the environment. When time is considered in studies of intraspecific trait ecology, the degree of variability in timing within a population becomes a key factor structuring trait-mediated ecological interactions and community processes.

Latitudinal resource gradient shapes multivariate defense strategies in a long-lived shrub.

Plant defense against herbivores is multidimensional, and investment into different defense traits is intertwined due to genetic, physiological, and ecological costs. This relationship is expected to generate a trade-off between direct defense and tolerance that is underlain by resource availability, with increasing resources being associated with increased investment in tolerance and decreased investment in direct resistance. We tested these predictions across populations of the shrub Artemisia californica by growing plants sourced from a latitudinal aridity gradient within common gardens located at the southern (xeric) and northern (mesic) portions of its distribution. We measured plant growth rate, resistance via a damage survey, and tolerance to herbivory by experimentally simulating vertebrate herbivory. Plants from more northern (vs. southern) environments were less resistant (received higher percent damage by vertebrate herbivores) and tended to be more tolerant (marginally significant) with respect to change in biomass measured 12 months after simulated vertebrate herbivory. Also, putative growth and defense traits paralleled patterns of resistance and tolerance, such that leaves from northern populations contained lower concentrations of terpenes and increased N, specific leaf area, and % water. Last, plant growth rate did not demonstrate clear clinal patterns, as northern populations (vs. southern populations) grew more slowly in the southern (xeric) garden, but there was no clinal relationship detected in the northern (mesic) garden. Overall, our findings support the prediction of lower resistance and higher tolerance in plant populations adapted to more resource-rich, mesic environments, but this trade-off was not associated with concomitant trade-offs in growth rate. These findings ultimately suggest that plant adaptation to resource availability and herbivory can shape intraspecific variation in multivariate plant defenses.

Snow melt timing acts independently and in conjunction with temperature accumulation to drive subalpine plant phenology.

Organisms use environmental cues to align their phenology-the timing of life events-with sets of abiotic and biotic conditions that favor the successful completion of their life cycle. Climate change has altered the environmental cues organisms use to track climate, leading to shifts in phenology with the potential to affect a variety of ecological processes. Understanding the drivers of phenological shifts is critical to predicting future responses, but disentangling the effects of temperature from precipitation on phenology is often challenging because they tend to covary. We addressed this knowledge gap in a high-elevation environment where phenological shifts are associated with both the timing of spring snow melt and temperature. We factorially crossed early snow melt and passive warming treatments to (1) disentangle the effects of snow melt timing and warming on the phenology of flowering and fruiting and reproductive success in three subalpine plant species (Delphinium nuttallianum, Valeriana edulis, and Potentilla pulcherrima); and (2) assess whether snow melt acts via temperature accumulation or some other aspect of the environment (e.g., soil moisture) to affect phenological events. Both the timing and duration of flowering and fruiting responded to the climate treatments, but the effect of snow melt timing and warming varied among species and phenological stages. The combined effects of the treatments on phenology were always additive, and the snow melt treatment often affected phenology even when the warming treatment did not. Despite marked responses of phenology to climate manipulations, the species showed little change in reproductive success, with only one species producing fewer seeds in response to warming (Delphinium, -56%). We also found that snow melt timing can act both through temperature accumulation and as a distinct cue for phenology, and these effects are not mutually exclusive. Our results show that one environmental cue, here snow melt timing, may act through multiple mechanisms to shift phenology.

Climatic displacement exacerbates the negative impact of drought on plant performance and associated arthropod abundance.

Climate change is acting on species and modifying communities and ecosystems through changes not only with respect to mean abiotic conditions, but also through increases in the frequency and severity of extreme events. Changes in mean aridity associated with climate change can generate ecotype by environment mismatch (i.e., climatic displacement). At the same time, variability around these shifting means is predicted to increase, resulting in more extreme droughts. We characterized the effects of two axes of climate change, climatic displacement and drought, on the shrub Artemisia californica and its arthropods. We established common gardens of plants sourced along an aridity gradient (3.5-fold variation in mean annual precipitation) in an arid region of the species distribution, thus generating a gradient of climatic displacement (sustained increase in aridity) as predicted with climate change. We surveyed plants and arthropods over eight years where precipitation varied sixfold, including both extreme drought and relatively mesic conditions. These two axes of climate change interacted to influence plant performance, such that climatically displaced populations grew slowly regardless of drought and suffered substantial mortality during drought years. Conversely, local populations grew quickly, increased growth during wet years, and had low mortality regardless of drought. Effects on plant annual arthropod yield were negative and additive, with drought effects exceeding that of climatic displacement by 24%. However, for plant lifetime arthropod yield, incorporating effects on both plant growth and survival, climatic displacement exacerbated the negative effects of drought. Collectively these results demonstrate how climatic displacement (through increasing aridity stress) strengthens the negative effects of drought on plants and, indirectly, on arthropods, suggesting the possibility of climate-mediated trophic collapse.

Generalising indirect defence and resistance of plants.

Indirect defence, the adaptive top-down control of herbivores by plant traits that enhance predation, is a central component of plant-herbivore interactions. However, the scope of interactions that comprise indirect defence and associated ecological and evolutionary processes has not been clearly defined. We argue that the range of plant traits that mediate indirect defence is much greater than previously thought, and we further organise major concepts surrounding their ecological functioning. Despite the wide range of plant traits and interacting organisms involved, indirect defences show commonalities when grouped. These categories are based on whether indirect defences boost natural enemy abundance via food or shelter resources, or, alternatively, increase natural enemy foraging efficiency via information or alteration of habitat complexity. The benefits of indirect defences to natural enemies should be further explored to establish the conditions in which indirect defence generates a plant-natural enemy mutualism. By considering the broader scope of plant-herbivore-natural enemy interactions that comprise indirect defence, we can better understand plant-based food webs, as well as the evolutionary processes that have shaped them.

Dietary specialization is conditionally associated with increased ant predation risk in a temperate forest caterpillar community.

The enemy-free space hypothesis (EFSH) contends that generalist predators select for dietary specialization in insect herbivores. At a community level, the EFSH predicts that dietary specialization reduces predation risk, and this pattern has been found in several studies addressing the impact of individual predator taxa or guilds. However, predation at a community level is also subject to combinatorial effects of multiple-predator types, raising the question of how so-called multiple-predator effects relate to dietary specialization in insect herbivores. Here, we test the EFSH with a field experiment quantifying ant predation risk to insect herbivores (caterpillars) with and without the combined predation effects of birds. Assessing a community of 20 caterpillar species, we use model selection in a phylogenetic comparative framework to identify the caterpillar traits that best predict the risk of ant predation. A caterpillar species' abundance, dietary specialization, and behavioral defenses were important predictors of its ant predation risk. Abundant caterpillar species had increased risk of ant predation irrespective of bird predation. Caterpillar species with broad diet breadth and behavioral responsiveness to attack had reduced ant predation risk, but these ant effects only occurred when birds also had access to the caterpillar community. These findings suggest that ant predation of caterpillar species is density- or frequency-dependent, that ants and birds may impose countervailing selection on dietary specialization within the same herbivore community, and that contingent effects of multiple predators may generate behaviorally mediated life-history trade-offs associated with herbivore diet breadth.

Sexual and genotypic variation in terpene quantitative and qualitative profiles in the dioecious shrub Baccharis salicifolia.

Terpenoids are secondary metabolites produced in most plant tissues and are often considered toxic or repellent to plant enemies. Previous work has typically reported on intra-specific variation in terpene profiles, but the effects of plant sex, an important axis of genetic variation, have been less studied for chemical defences in general, and terpenes in particular. In a prior study, we found strong genetic variation (but not sexual dimorphism) in terpene amounts in leaves of the dioecious shrub Baccharis salicifolia. Here we build on these findings and provide a more in-depth analysis of terpene chemistry on these same plants from an experiment consisting of a common garden with male (N = 19) and female (N = 20) genotypes sourced from a single population. Our goal in the present study was to investigate quantitative and qualitative differences in terpene profiles associated with plant sex and genotypic variation. For this, we quantified leaf mono- and sesquiterpene amount, richness, and diversity (quantitative profile), as well as the composition of compounds (qualitative profile). We found no evidence of sexual dimorphism in monoterpene or sesquiterpene profiles. We did, however, find significant genotypic variation in amount, diversity, and composition of monoterpenes, but no effects on sesquiterpenes. These findings indicated that genotypic variation in terpene profiles largely surpassed variation due to sexual dimorphism for the studied population of this species.

Plant structural complexity mediates trade-off in direct and indirect plant defense by birds.

Direct and indirect defenses are predicted to trade-off due to costs associated with redundancy in plant defense, but the factors mediating a plant's position along this trade-off axis are unknown. We conducted a bird exclusion experiment of nine sympatric shrub species to assess convergent associations among direct defense, indirect defense from birds, and shrub structural complexity, a trait predicted to influence bird foraging. We found high variation in defense; direct resistance varied four-fold, with indirect defense ranging from a 59% reduction to a 32% increase in herbivore density. These resistance strategies traded off and were mediated by plant structure; high complexity was associated with weaker indirect defense from birds, strong direct defense, and more predatory arthropods. Our findings suggest that species with growth forms that inhibit bird foraging invest more in direct defense and may provide refuge for arthropod predators. Accordingly, we provide evidence for a potentially widespread mechanism underlying the evolution of plant defenses.

Plant chemical mediation of ant behavior.

Ants are ecologically dominant members of terrestrial communities. Ant foraging is often strongly associated with plants and depends upon associative learning of chemicals in the environment. As a result, plant chemicals can affect ant behaviors and, in so doing, have strong multi-trophic indirect effects. Plant chemicals mediate ant behaviors in the contexts of floral visitation, seed dispersal and predation, leaf cutting, interactions with ant-mutualist host plants, interactions with mutualist and prey insects in plant canopies, and plant predation of ants by carnivorous plants. Here, we review what is known about these differing contexts in which plant chemicals influence ant behavior, the mechanisms by which ants are affected by plant chemicals, and future directions within these topics.

Elevational cline in herbivore abundance driven by a monotonic increase in trophic-level sensitivity to aridity.

The abiotic environment drives species abundances and distributions both directly and indirectly through effects on multi-trophic species interactions. However, few studies have documented the individual and combined consequences of these direct and indirect effects. We studied an ant-tended aphid along an elevational gradient, where lower elevations were more arid. Hypotheses of stronger species interactions at lower elevations and a greater sensitivity of higher trophic levels to climate led us to predict increased top-down control of aphids by natural enemies (third trophic level) but even stronger protection from mutualist ants (fourth trophic level) with increasing aridity. As a result, we predicted that mutualism strength and aphid abundance would increase with aridity. We documented patterns of aphid abundance and tested for both the direct and multi-trophic indirect effects of aridity on aphid performance. To do so, we used both observational and manipulative methods across two years in replicate high- and low-elevation valleys, where summer temperatures decreased by 3.7°C and precipitation increased by 27 mm/mo from low to high elevations. Aphid colonies were 75% larger in the most (vs. least) arid sites, and this was best explained by changes in interactions with predators and ants. Aphids were unaffected by the direct effects of the abiotic environment or its indirect effects via host plant quality. In contrast, natural enemy effects increased with aridity; under ant exclusion, natural enemies had no effect on aphids in the least arid sites but depressed colony growth by 252% in the most arid sites. Ant activity also increased with aridity, with ants discovering more aphid colonies and experimental baits and allocating more foragers per aphid, although there was no effect of aridity on ant abundance or community composition. Correspondingly, the mutualist services provided by ants increased with aridity; ants provided no benefits to aphids in the least arid sites but doubled colony growth in the most arid sites. In summary, an elevational cline in herbivore abundance was driven by a monotonic increase in trophic-level sensitivity to aridity. These findings illustrate that predicting species responses to climate change will require a multi-trophic perspective.

Weather cues associated with masting behavior dampen the negative autocorrelation between past and current reproduction in oaks.

PREMISE OF THE STUDY: The influence of weather conditions on masting and the ecological advantages of this reproductive behavior have been the subject of much interest. Weather conditions act as cues influencing reproduction of individual plants, and similar responses expressed across many individuals lead to population-level synchrony in reproductive output. In turn, synchrony leads to benefits from economies of scale such as enhanced pollination success and seed predator satiation. However, there may also be individual-level benefits from reproductive responses to weather cues, which may explain the origin of masting in the absence of economies of scale. In a previous study, we found support for a mechanism whereby individual responses to weather cues attenuate the negative autocorrelation between past and current annual seed production-a pattern typically attributed to resource limitation and reproductive tradeoffs among years. METHODS: Here we provide a follow-up and more robust evaluation of this hypothesis in 12 species of oaks (Quercus spp.), testing for a negative autocorrelation (tradeoff) between past and current reproduction and whether responses to weather cues associated with masting reduce the strength of this negative autocorrelation. KEY RESULTS: Our results showed a strong negative autocorrelation for 11 of the species, and that species-specific reproductive responses to weather cues dampened this negative autocorrelation in 10 of them. CONCLUSIONS: This dampening effect presumably reflects a reduction in resource limitation or increased resource use associated with weather conditions, and suggests that responses to weather cues conferring these advantages should be selected for based on individual benefits.

Specificity of plant-plant communication for Baccharis salicifolia sexes but not genotypes.

Plants are able to adjust their anti-herbivore defenses in response to the volatile organic compounds (VOCs) emitted by herbivore-damaged neighbors, and some of these changes increase resistance against subsequent herbivory. This phenomenon of plant-plant communication is thought to be widespread, but recent investigations have cautioned that it can be context dependent, including variation in the strength of communication based on the identity of plants and their associated herbivores. Here, we performed three greenhouse experiments using multiple male and female genotypes of the dioecious woody shrub Baccharis salicifolia and its specialist aphid Uroleucon macolai to test for specificity of plant-plant communication with respect to plant sex and genotype. Moreover, we evaluated plant sexual dimorphism and genotypic variation in VOC emissions (i.e., the "speaking" side of the interaction) and response of plants to VOC exposure (i.e., the "listening" side of the interaction) in order to identify the chemical mechanisms underlying such specificity. We did not find genotypic specificity of communication; emitter plants damaged by U. macolai significantly reduced subsequent U. macolai performance on receivers, but these effects were indistinguishable for communication within vs. among genotypes. In contrast, we found sex specificity of communication; male emitter plants reduced subsequent U. macolai performance on male and female receiver plants equally, while female emitter plants only did so for female receivers. We found sexual (but not genotypic) dimorphism in speaking but not listening; of the seven compounds induced by U. macolai feeding (speaking), pinocarvone was approximately fivefold greater in female than in male plants, while exposure of plants to pinocarvone emissions (listening) reduced U. macolai performance equally in both male and female plants. Together, our study demonstrates novel evidence for sexually dimorphic specificity of plant-plant communication and the chemical mechanism underlying this effect.

Tropical tree diversity mediates foraging and predatory effects of insectivorous birds.

Biodiversity affects the structure of ecological communities, but little is known about the interactive effects of diversity across multiple trophic levels. We used a large-scale forest diversity experiment to investigate the effects of tropical tree species richness on insectivorous birds, and the subsequent indirect effect on predation rates by birds. Diverse plots (four tree species) had higher bird abundance (61%), phylogenetic diversity (61%), and functional diversity (55%) than predicted based on single-species monocultures, which corresponded to higher attack rates on artificial caterpillars (65%). Tree diversity effects on attack rate were driven by complementarity among tree species, with increases in attack rate observed on all tree species in polycultures. Attack rates on artificial caterpillars were higher in plots with higher bird abundance and diversity, but the indirect effect of tree species richness was mediated by bird diversity, providing evidence that diversity can interact across trophic levels with consequences tied to ecosystem services and function.

A test for clinal variation in Artemisia californica and associated arthropod responses to nitrogen addition.

The response of plant traits to global change is of fundamental importance to understanding anthropogenic impacts on natural systems. Nevertheless, little is known about plant genetic variation in such responses or the indirect effect of environmental change on higher trophic levels. In a three-year common garden experiment, we grew the shrub Artemisia californica from five populations sourced along a 700 km latitudinal gradient under ambient and nitrogen (N) addition (20 kg N ha-1) and measured plant traits and associated arthropods. N addition increased plant biomass to a similar extent among all populations. In contrast, N addition effects on most other plant traits varied among plant populations; N addition reduced specific leaf area and leaf percent N and increased carbon to nitrogen ratios in the two northern populations, but had the opposite or no effect on the three southern populations. N addition increased arthropod abundance to a similar extent among all populations in parallel with an increase in plant biomass, suggesting that N addition did not alter plant resistance to herbivores. N addition had no effect on arthropod diversity, richness, or evenness. In summary, genetic variation among A. californica populations mediated leaf-trait responses to N addition, but positive direct effects of N addition on plant biomass and indirect effects on arthropod abundance were consistent among all populations.

Relative effects of genetic variation sensu lato and sexual dimorphism on plant traits and associated arthropod communities.

Intraspecific plant trait variation can have cascading effects on plant-associated biotic communities. Sexual dimorphism is an important axis of genetic variation in dioecious plants, but the strength of such effects and the underlying mechanisms relative to genetic variation are unknown. We established a common garden with 39 genotypes of Baccharis salicifolia sampled from a single population that included male and female genotypes and measured plant traits and quantified associated arthropod communities. Genetic variation sensu lato (genotypic variation) had strong effects on most plant traits (flower number, relative growth rate, specific leaf area, percent water content, carbon-nitrogen ratio, monoterpene but not sesquiterpene concentrations) and on herbivore and predator density, and on arthropod community composition (relative abundance of 14 orders). In contrast, sexual dimorphism had weaker effects on only a few plant traits (flower number and relative growth rate), on predator density, and on arthropod community composition, but had no effect on herbivore density. Variation in flower number drove genetic variation sensu lato and sex dimorphism in predator density and arthropod community composition. There was unique genetic variation sensu lato in herbivore density (positively) associated with monoterpene concentration and in arthropod community composition associated with specific leaf area and carbon-nitrogen ratio. There was unique sexual dimorphism in arthropod community composition associated with plant relative growth rate. Together, these results demonstrate that genetic variation sensu lato and sexual dimorphism can shape plant-associated arthropod communities via both parallel and unique mechanisms, with greater overall effects of the former.

Intra-Specific Latitudinal Clines in Leaf Carbon, Nitrogen, and Phosphorus and their Underlying Abiotic Correlates in Ruellia Nudiflora.

While plant intra-specific variation in the stoichiometry of nutrients and carbon is well documented, clines for such traits have been less studied, despite their potential to reveal the mechanisms underlying such variation. Here we analyze latitudinal variation in the concentration of leaf nitrogen (N), phosphorus (P), carbon (C) and their ratios across 30 populations of the perennial herb Ruellia nudiflora. In addition, we further determined whether climatic and soil variables underlie any such latitudinal clines in leaf traits. The sampled transect spanned 5° latitude (ca. 900 km) and exhibited a four-fold precipitation gradient and 2 °C variation in mean annual temperature. We found that leaf P concentration increased with precipitation towards lower latitudes, whereas N and C did not exhibit latitudinal clines. In addition, N:P and C:P decreased towards lower latitudes and latitudinal variation in the former was weakly associated with soil conditions (clay content and cation exchange capacity); C:N did not exhibit a latitudinal gradient. Overall, these results emphasize the importance of addressing and disentangling the simultaneous effects of abiotic factors associated with intra-specific clines in plant stoichiometric traits, and highlight the previously underappreciated influence of abiotic factors on plant nutrients operating under sharp abiotic gradients over smaller spatial scales.