Individual tree traits shape insect and disease damage on oak in a climate‐matching tree diversity experiment

Diversifying planted forests by increasing genetic and species diversity is often promoted as a method to improve forest resilience to climate change and reduce pest and pathogen damage. In this study, we used a young tree diversity experiment replicated at two sites in the UK to study the impacts of tree diversity and tree provenance (geographic origin) on the oak (Quercus robur) insect herbivore community and a specialist biotrophic pathogen, oak powdery mildew. Local UK, French, and Italian provenances were planted in monocultures, provenance mixtures, and species mixes, allowing us to test whether: (a) local and nonlocal provenances differ in their insect herbivore and pathogen communities, and (b) admixing trees leads to associational effects on insect herbivore and pathogen damage. Tree diversity had variable impacts on foliar organisms across sites and years, suggesting that diversity effects can be highly dependent on environmental context. Provenance identity impacted upon both herbivores and powdery mildew, but we did not find consistent support for the local adaptation hypothesis for any group of organisms studied. Independent of provenance, we found tree vigor traits (shoot length, tree height) and tree apparency (the height of focal trees relative to their surroundings) were consistent positive predictors of powdery mildew and insect herbivory. Synthesis. Our results have implications for understanding the complex interplay between tree identity and diversity in determining pest damage, and show that tree traits, partially influenced by tree genotype, can be important drivers of tree pest and pathogen loads.     

Bottom‐up vs. top‐down effects on terrestrial insect herbivores: a meta‐analysis

Primary consumers are under strong selection from resource (‘bottom‐up’) and consumer (‘top‐down’) controls, but the relative importance of these selective forces is unknown. We performed a meta‐analysis to compare the strength of top‐down and bottom‐up forces on consumer fitness, considering multiple predictors that can modulate these effects: diet breadth, feeding guild, habitat/environment, type of bottom‐up effects, type of top‐down effects and how consumer fitness effects are measured. We focused our analyses on the most diverse group of primary consumers, herbivorous insects, and found that in general top‐down forces were stronger than bottom‐up forces. Notably, chewing, sucking and gall‐making herbivores were more affected by top‐down than bottom‐up forces, top‐down forces were stronger than bottom‐up in both natural and controlled (cultivated) environments, and parasitoids and predators had equally strong top‐down effects on insect herbivores. Future studies should broaden the scope of focal consumers, particularly in understudied terrestrial systems, guilds, taxonomic groups and top‐down controls (e.g. pathogens), and test for more complex indirect community interactions. Our results demonstrate the surprising strength of forces exerted by natural enemies on herbivorous insects, and thus the necessity of using a tri‐trophic approach when studying insect‐plant interactions.     

Bottom‐up and top‐down effects of browning and warming on shallow lake food webs

Productivity and trophic structure of aquatic ecosystems result from a complex interplay of bottom‐up and top‐down forces that operate across benthic and pelagic food web compartments. Projected global changes urge the question how this interplay will be affected by browning (increasing input of terrestrial dissolved organic matter), nutrient enrichment and warming. We explored this with a process‐based model of a shallow lake food web consisting of benthic and pelagic components (abiotic resources, primary producers, grazers, carnivores), and compared model expectations with the results of a browning and warming experiment in nutrient‐poor ponds harboring a boreal lake community. Under low nutrient conditions, the model makes three major predictions. (a) Browning reduces light and increases nutrient supply; this decreases benthic and increases pelagic production, gradually shifting productivity from the benthic to the pelagic habitat. (b) Because of active habitat choice, fish exert top‐down control on grazers and benefit primary producers primarily in the more productive of the two habitats. (c) Warming relaxes top‐down control of grazers by fish and decreases primary producer biomass, but effects of warming are generally small compared to effects of browning and nutrient supply. Experimental results were consistent with most model predictions for browning: light penetration, benthic algal production, and zoobenthos biomass decreased, and pelagic nutrients and pelagic algal production increased with browning. Also consistent with expectations, warming had negative effects on benthic and pelagic algal biomass and weak effects on algal production and zoobenthos and zooplankton biomass. Inconsistent with expectations, browning had no effect on zooplankton and warming effects on fish depended on browning. The model is applicable also to nutrient‐rich systems, and we propose that it is a useful tool for the exploration of the consequences of different climate change scenarios for productivity and food web dynamics in shallow lakes, the worldwide most common lake type.     

Variable strength of top‐down effects in Nothofagus forests: bird predation and insect herbivory during an ENSO event

Abstract Predators are thought to play a key role in controlling herbivory, thus having positive indirect effects on plants. However, evidence for terrestrial trophic cascades is still fragmentary, perhaps due to variation in top‐down forces created by environmental heterogeneity. We examined the magnitude of predation effects on foliar damage by chewing insects and mean leaf size, by excluding birds from saplings in ‘dry’ and ‘wet’Nothofagus pumilio forests in the northern Patagonian Andes, Argentina. The experiment lasted 2 years encompassing a severe drought during the La Niña phase of a strong El Niño/Southern Oscillation event, which was followed by unusually high background folivory levels. Insect damage was consistently higher in wet than in dry forest saplings. In the drought year (1999), bird exclusion increased folivory rates in both forests but did not affect tree leaf size. In the ensuing season (2000), leaf damage was generally twice as high as in the drought year. As a result, bird exclusion not only increased the extent of folivory but also significantly decreased sapling leaf size. The latter effect was stronger in the wet forest, suggesting compensation of leaf area loss by dry forest saplings. Overall, the magnitude of predator indirect effects depended on the response variable measured. Insectivorous birds were more effective at reducing folivory than at facilitating leaf area growth. Our results indicate that bird‐initiated trophic cascades protect N. pumilio saplings from insect damage even during years with above‐normal herbivory, and also support the view that large‐scale climatic events influence the strength of trophic cascades.     

Resource–consumer diversity: testing the effects of leaf litter species diversity on stream macroinvertebrate communities

1. Understanding relationships between resource and consumer diversity is essential to predicting how changes in resource diversity might affect several trophic levels and overall ecosystem functioning. 2. We tested for the effects of leaf litter species diversity (i.e. litter mixing) on litter mass remaining and macroinvertebrate communities (taxon diversity, abundance and biomass) during breakdown in a detritus‐based headwater stream (North Carolina, U.S.A.). We used full‐factorial analyses of single‐ and mixed‐species litter from dominant riparian tree species with distinct leaf chemistries [red maple (Acer rubrum), tulip poplar (Liriodendron tulipifera), chestnut oak (Quercus prinus) and rhododendron (Rhododendron maximum)] to test for additivity (single‐species litter presence/absence effects) and non‐additivity (emergent effects of litter species interactions). 3. Significant non‐additive effects of litter mixing on litter mass remaining were explained by species composition, but not richness, and litter‐mixing effects were variable throughout breakdown. Specifically, small differences in observed versus expected litter mass remaining were measured on day 14; whereas observed litter mass remaining in mixed‐species leaf packs was significantly higher on day 70 and lower on day 118 than expected from data for single‐species leaf packs. 4. Litter mixing had non‐additive effects on macroinvertebrate community structure. The number of species in litter mixtures (two to four), but not litter species composition, was a significant predictor of the dominance of particular macroinvertebrates (i.e. indicator taxa) within mixed‐species packs. 5. In addition, the presence/absence of high‐ (L. tulipifera) and low‐quality (R. maximum) litter had additive effects on macroinvertebrate taxon richness, abundance and biomass. The presence of L. tulipifera litter had both positive (synergistic) and negative (antagonistic) effects on invertebrate taxon richness, that varied during breakdown but were not related to litter chemistry. In contrast, the presence/absence of L. tulipifera had a negative relationship with total macroinvertebrate biomass (due to low leaf mass remaining when L. tulipifera was present and higher condensed and hydrolysable tannins associated with leaf packs lacking L. tulipifera). Macroinvertebrate abundance was consistently lower when R. maximum was present, which was partially explained by litter chemistry [e.g., high concentrations of lignin, condensed tannins, hydrolysable tannins and total phenolics and high carbon to nutrient (N and P) ratios]. 6. The bottom‐up effects of litter species diversity on stream macroinvertebrates and litter breakdown are different, which suggests that structural attributes of macroinvertebrate communities may only partially explain the effects of litter‐mixing on organic matter processing in streams. In addition, stream macroinvertebrates colonising decomposing litter are influenced by resource diversity as well as resource availability. Broad‐scale shifts in riparian tree species composition will alter litter inputs to streams, and our results suggest that changes in the diversity and availability of terrestrial litter may alter stream food webs and organic matter processing.     

Bottom–up and top–down effects on plant communities: nutrients limit productivity,but insects determine diversity and composition

Top–down effects of herbivores and bottom–up effects of nutrients shape productivity and diversity across ecosystems, yet their single and combined effects on spatial and temporal beta diversity is unknown. We established a field experiment in which the abundance of insect herbivores (top–down) and soil nitrogen (bottom–up) were manipulated over six years in an existing old‐field community. We tracked plant α and β diversity – within plot richness and among plot biodiversity‐ and aboveground net primary productivity (ANPP) over the course of the experiment. We found that bottom–up factors affected ANPP while top–down factors influenced plant community structure. Across years, while N reduction lowered ANPP by 10%, N reduction did not alter ANPP relative to control plots. Further, N reduction lowered ANPP by 20% relative to N addition plots. On the other hand, the reduction of insect herbivores did not alter plant richness (α diversity) yet consistently promoted Shannon's evenness, relative to plots where insect herbivores were present. Further, insect herbivores promoted spatial‐temporal β diversity. Overall, we found that the relative importance of top–down and bottom–up controls of plant ANPP, plant α diversity, and composition (β diversity) can vary significantly in magnitude and direction. In addition, their effects varied through time, with bottom–up effects influencing ANPP quickly while the effects of top–down factors emerging only late in the experiment to influence plant community composition via shifts in plant dominance.     

Shade tolerance and herbivory are associated with RGR of tree species via different functional traits

• Relative growth rate (RGR) plays an important role in plant adaptation to the light environment through the growth potential/survival trade‐off. RGR is a complex trait with physiological and biomass allocation components. It has been argued that herbivory may influence the evolution of plant strategies to cope with the light environment, but little is known about the relation between susceptibility to herbivores and growth‐related functional traits.
• Here, we examined in 11 evergreen tree species from a temperate rainforest the association between growth‐related functional traits and (i) species’ shade‐tolerance, and (ii) herbivory rate in the field. We aimed at elucidating the differential linkage of shade and herbivory with RGR via growth‐related functional traits.
• We found that RGR was associated negatively with shade‐tolerance and positively with herbivory rate. However, herbivory rate and shade‐tolerance were not significantly related. RGR was determined mainly by photosynthetic rate (A_max) and specific leaf area (SLA). Results suggest that shade tolerance and herbivore resistance do not covary with the same functional traits. Whereas shade‐tolerance was strongly related to A_max and to a lesser extent to leaf mass ratio (LMR) and dark respiration (R_d), herbivory rate was closely related to allocation traits (SLA and LMR) and slightly associated with protein content.
• The effects of low light on RGR would be mediated by A_max, while the effects of herbivory on RGR would be mediated by SLA. Our findings suggest that shade and herbivores may differentially contribute to shape RGR of tree species through their effects on different resource‐uptake functional traits.

     

Elevated CO2 decreases leaf fluctuating asymmetry and herbivory by leaf miners on two oak species

Fluctuating asymmetry (FA) represents small, random variation from symmetry in otherwise bilaterally symmetrical characters. Significant increases in FA have been found for several species of plants and animals in response to various stresses, including environmental and genetic factors. In this study, we investigated the effects of elevated CO₂ on leaf symmetry of two oak species, Quercus geminata and Q. myrtifolia, and the responses of three species of leaf miners and one gall‐making species to random variation in leaf morphology. Leaf FA decreased with an increase in CO₂ concentration. There were fewer asymmetric leaves and lower levels of asymmetry on leaf width and leaf area on elevated CO₂ compared with ambient CO₂. Leaf miners responded to leaf asymmetry, attacking asymmetric leaves more frequently than expected by chance alone. Differences in secondary chemistry and nitrogen (N) content between symmetric and asymmetric leaves may be responsible for these results due to lower levels of tannins and higher levels of N found on asymmetric leaves of Q. myrtifolia and Q. geminata.     

Direct and indirect top‐down effects of previous contact with an enemy on the feeding behavior of blowfly larvae

We investigated the addition of a trophic level to a simple food web. Direct and indirect effects caused by the presence of a new species in the food web were quantified by estimating survival and consumption rates on the basal resource. We focused on a blowfly intraguild prey–predator system with various ecological interactions taking place during the larval period. The experiments were designed to set Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae) as the intraguild prey and Chrysomya albiceps (Wiedemann) as the intraguild predator and/or cannibal. The generalist pupal parasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) was introduced into the system during a non‐susceptible life stage of the interacting blowfly species. The cascading parasitoid effects induced behavioral changes in the blowfly larvae, increasing the impact of intraguild predation and cannibalism on blowfly survival. The results suggest that blowfly larvae can change their feeding behavior in response to the presence of a parasitoid.     

The effect of top‐predator presence and phenotype on aquatic microbial communities

The presence of predators can impact a variety of organisms within the ecosystem, including microorganisms. Because the effects of fish predators and their phenotypic differences on microbial communities have not received much attention, we tested how the presence/absence, genotype, and plasticity of the predatory three‐spine stickleback (Gasterosteus aculeatus) influence aquatic microbes in outdoor mesocosms. We reared lake and stream stickleback genotypes on contrasting food resources to adulthood, and then added them to aquatic mesocosm ecosystems to assess their impact on the planktonic bacterial community. We also investigated whether the effects of fish persisted following the removal of adults, and the subsequent addition of a homogenous juvenile fish population. The presence of adult stickleback increased the number of bacterial OTUs and altered the size structure of the microbial community, whereas their phenotype affected bacterial community composition. Some of these effects were detectable after adult fish were removed from the mesocosms, and after juvenile fish were placed in the tanks, most of these effects disappeared. Our results suggest that fish can have strong short‐term effects on microbial communities that are partially mediated by phenotypic variation of fish.     

Priority effects are interactively regulated by top‐down and bottom‐up forces: evidence from wood decomposer communities

Both top‐down (grazing) and bottom‐up (resource availability) forces can determine the strength of priority effects, or the effects of species arrival history on the structure and function of ecological communities, but their combined influences remain unresolved. To test for such influences, we assembled experimental communities of wood‐decomposing fungi using a factorial manipulation of fungivore (Folsomia candida) presence, nitrogen availability, and fungal assembly history. We found interactive effects of all three factors on fungal species composition and wood decomposition 1 year after the fungi were introduced. The strength of priority effects on community structure was affected primarily by nitrogen availability, whereas the strength of priority effects on decomposition rate was interactively regulated by nitrogen and fungivores. These results demonstrate that top‐down and bottom‐up forces jointly determine how strongly assembly history affects community structure and function.     

Functional identity is the main driver of diversity effects in young tree communities

Two main effects are proposed to explain biodiversity–ecosystem functioning relationships: niche complementarity and selection effects. Both can be functionally defined using the functional diversity (FD) and functional identity (FI) of the community respectively. Herein, we present results from the first tree diversity experiment that separated the effect of selection from that of complementarity by varying community composition in high‐density plots along a gradient of FD, independent of species richness and testing for the effects of FD and community weighted means of traits (a proxy for FI) on stem biomass increment (a proxy for productivity). After 4 years of growth, most mixtures did not differ in productivity from the averages of their respective monocultures, but some did overyield significantly. Those positive diversity effects resulted mostly from selection effects, primarily driven by fast‐growing deciduous species and associated traits. Net diversity effect did not increase with time over 4 years.     

Quantifying the effects of drought on abrupt growth decreases of major tree species in Switzerland

Drought entails important effects on tree physiology, which may result in short‐ to long‐term radial growth decreases. While the majority of studies have focused on annual drought‐related variability of growth, relatively little is known about sustained growth decreases following drought years. We apply a statistical framework to identify climatic factors that induce abrupt growth decreases and may eventually result in tree mortality. We used tree‐ring data from almost 500 standing dead trees and 200 living trees in eight sites of the Swiss network of strict forest reserves, including four of the most important Central European tree species (Abies alba, Picea abies, Fagus sylvatica and Quercus spp.). First, to assess short‐term growth responses to drought under various climate and site conditions, we calculated correlations and linear mixed‐effects models between ring‐width indices (RWIs) and drought based on the Standardized Precipitation Evapotranspiration Index (SPEI). Second, to quantify drought effects on abrupt growth decreases, we applied distributed lag nonlinear models (DLNMs), which account for both delayed effects and the nonlinear relationship between the SPEI and the occurrence of abrupt growth decreases. Positive correlations between RWIs and the SPEI indicated short‐term growth responses of all species, particularly at arid sites. Results of the DLNMs revealed species‐specific growth responses to drought. For Quercus spp., abrupt growth decreases were more likely to occur several years following severe drought, whereas for P. abies, A. alba, and F. sylvatica abrupt growth decreases started frequently immediately in the drought year. We conclude that the statistical framework allows for quantifying the effects of drought intensity on the probability of abrupt growth decreases, which ultimately contributes to an improved understanding of climate impacts on forest community dynamics.     

Testing top‐down and bottom‐up effects on arid zone beetle assemblages following mammal reintroduction

Species extinctions and declines are occurring globally and commonly have cascading effects on ecosystems. In Australia, mammal extinctions have been extensive, particularly in arid areas, where precipitation drives ecosystems. Many ecologically extinct mammals feed on soil‐dwelling insects. However, how this top‐down pressure affected their prey and how this contrasts with the bottom‐up impacts of fluctuating precipitation remains unclear. We constructed a long‐term exclusion experiment in a multi‐species mammal reintroduction zone in semi‐arid Australia to test how top‐down (reintroduced mammals) and bottom‐up (precipitation) factors affect root‐feeding chafer beetles (Coleoptera: Melolonthinae). We used emergence traps in ten replicate 20 × 20 m plots of control, exclusion and procedural control treatments to trap chafers biannually from 2009 to 2015. Annual precipitation during this period varied from 173 to 481 mm. Mammal exclusion did not affect chafers, indicating that top‐down regulation was not important. Instead, chafer abundance, species density and biomass increased with precipitation. Chafer body size and assemblage composition were best predicted by sampling year, suggesting that random drift determined species abundances. Increased resource availability therefore favoured all species similarly. We thus found no evidence that mammal predation alters chafer populations and conclude that they may be driven primarily by bottom‐up processes. Further research should determine if the cascading effects of species loss are less important for herbivores generally than for higher level trophic groups and the role of ecosystem stability in mediating these patterns.     

Leaf traits and herbivory rates of tropical tree species differing in successional status

We evaluated leaf characteristics and herbivory intensities for saplings of fifteen tropical tree species differing in their successional position. Eight leaf traits were selected, related to the costs of leaf display (specific leaf area [SLA], water content), photosynthesis (N and P concentration per unit mass), and herbivory defence (lignin concentration, C:N ratio). We hypothesised that species traits are shaped by variation in abiotic and biotic (herbivory) selection pressures along the successional gradient. All leaf traits varied with the successional position of the species. The SLA, water content and nutrient concentration decreased, and lignin concentration increased with the successional position. Herbivory damage (defined as the percentage of damage found at one moment in time) varied from 0.9-8.5% among the species, but was not related to their successional position. Herbivory damage appeared to be a poor estimator of the herbivory rate experienced by species, due to the confounding effect of leaf lifespan. Herbivory rate (defined as percentage leaf area removal per unit time) declined with the successional position of the species. Herbivory rate was only positively correlated to water content, and negatively correlated to lignin concentration, suggesting that herbivores select leaves based upon their digestibility rather than upon their nutritive value. Surprisingly, most species traits change linearly with succession, while resource availability (light, nutrients) declines exponentially with succession.     

Bottom–up regulates top–down: the effects of hybridization of grass endophytes on an aphid herbivore and its generalist predator

The ecological consequences of hybridization of microbial symbionts are largely unknown. We tested the hypothesis that hybridization of microbial symbionts of plants can negatively affect performance of herbivores and their natural enemies. In addition, we studied the effects of hybridization of these symbionts on feeding preference of herbivores and their natural enemies. We used Arizona fescue as the host‐plant, Neotyphodium endophytes as symbionts, the bird cherry–oat aphid as the herbivore and the pink spotted ladybird beetle as the predator in controlled experiments. Neither endophyte infection (infected or not infected) nor hybrid status (hybrid and non‐hybrid infection) affected aphid reproduction, proportion of winged forms in the aphid populations, aphid host‐plant preference or body mass of the ladybirds. However, development of ladybird larvae was delayed when fed with aphids grown on hybrid (H+) endophyte infected grasses compared to larvae fed with aphids from non‐hybrid (NH+) infected grasses, non‐hybrid, endophyte‐removed grasses (NH?) and hybrid, endophyte‐removed (H?) grasses. Furthermore, adult beetles were more likely to choose all other types of grasses harboring aphids rather than H+ infected grasses. In addition, development of ladybirds was delayed when fed with aphids from naturally uninfected (E?) grasses compared to ladybirds that were fed with aphids from NH+ and NH? grasses. Our results suggest that hybridization of microbial symbionts may negatively affect generalist predators such as the pink spotted ladybird and protect herbivores like the bird cherry–oat aphids from predation even though the direct effects on herbivores are not evident.