Leaf isotopes reveal tree diversity effects on the functional responses to the pan-European 2018 summer drought.

Recent droughts have strongly impacted forest ecosystems and are projected to increase in frequency, intensity, and duration in the future together with continued warming. While evidence suggests that tree diversity can regulate drought impacts in natural forests, few studies examine whether mixed tree plantations are more resistant to the impacts of severe droughts. Using natural variations in leaf carbon (C) and nitrogen (N) isotopic ratios, that is δ13C and δ15N, as proxies for drought response, we analyzed the effects of tree species richness on the functional responses of tree plantations to the pan-European 2018 summer drought in seven European tree diversity experiments. We found that leaf δ13C decreased with increasing tree species richness, indicating less drought stress. This effect was not related to drought intensity, nor desiccation tolerance of the tree species. Leaf δ15N increased with drought intensity, indicating a shift toward more open N cycling as water availability diminishes. Additionally, drought intensity was observed to alter the influence of tree species richness on leaf δ15N from weakly negative under low drought intensity to weakly positive under high drought intensity. Overall, our findings suggest that dual leaf isotope analysis helps understand the interaction between drought, nutrients, and species richness.

Does spatial variation in insect herbivory match variations in plant quality? A meta-analysis.

Variation in herbivore pressure has often been predicted from patterns in plant traits considered as antiherbivore defences. Here, we tested whether spatial variation in field insect herbivory is associated with the variation in plant quality by conducting a meta-analysis of 223 correlation coefficients between herbivory levels and the expression of selected plant traits. We found no overall correlation between herbivory and either concentrations of plant secondary metabolites or values of physical leaf traits. This result was due to both the large number of low correlations and the opposing directions of high correlations in individual studies. Field herbivory demonstrated a significant association only with nitrogen: herbivore pressure increased with an increase in nitrogen concentration in plant tissues. Thus, our meta-analysis does not support either theoretical prediction, i.e., that plants possess high antiherbivore defences in localities with high herbivore pressure or that herbivory is low in localities where plant defences are high. We conclude that information about putative plant defences is insufficient to predict plant losses to insects in field conditions and that the only bottom-up factor shaping spatial variation in insect herbivory is plant nutritive value. Our findings stress the need to improve a theory linking plant putative defences and herbivory.

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.

Microbial biomarkers of tree water status for next-generation biomonitoring of forest ecosystems.

Next-generation biomonitoring proposes to combine machine-learning algorithms with environmental DNA data to automate the monitoring of the Earth's major ecosystems. In the present study, we searched for molecular biomarkers of tree water status to develop next-generation biomonitoring of forest ecosystems. Because phyllosphere microbial communities respond to both tree physiology and climate change, we investigated whether environmental DNA data from tree phyllosphere could be used as molecular biomarkers of tree water status in forest ecosystems. Using an amplicon sequencing approach, we analysed phyllosphere microbial communities of four tree species (Quercus ilex, Quercus robur, Pinus pinaster and Betula pendula) in a forest experiment composed of irrigated and non-irrigated plots. We used these microbial community data to train a machine-learning algorithm (Random Forest) to classify irrigated and non-irrigated trees. The Random Forest algorithm detected tree water status from phyllosphere microbial community composition with more than 90% accuracy for oak species, and more than 75% for pine and birch. Phyllosphere fungal communities were more informative than phyllosphere bacterial communities in all tree species. Seven fungal amplicon sequence variants were identified as candidates for the development of molecular biomarkers of water status in oak trees. Altogether, our results show that microbial community data from tree phyllosphere provides information on tree water status in forest ecosystems and could be included in next-generation biomonitoring programmes that would use in situ, real-time sequencing of environmental DNA to help monitor the health of European temperate forest ecosystems.

Is ecology different when studied with citizen scientists? A bibliometric analysis.

Ecology is broad and relies on several complementary approaches to study the mechanisms driving the distribution and abundance of organisms and their interactions. One of them is citizen science (CitSci), the co-production of scientific data and knowledge by nonprofessional scientists, in collaboration with, or under the direction of, professional scientists. CitSci has bloomed in the scientific literature over the last decade and its popularity continues to increase, but its qualitative contribution to the development of academic knowledge remains understudied. We used a bibliometric analysis to study whether the epistemic content of CitSci-based articles is different from traditional, non-CitSci ones within the field of ecology. We analyzed keywords and abstracts of articles published in ecology over the last decade, disentangling CitSci articles (those explicitly referring to citizen science) and non-CitSci articles. Keyword co-occurrence and thematic map analyses first revealed that CitSci and non-CitSci articles broadly focused on biodiversity, conservation, and climate change. However, CitSci articles did so in a more descriptive way than non-CitSci articles, which were more likely to address mechanisms. Conservation biology and its links with socio-ecosystems and ecosystem services was a central theme in the CitSci corpus, much less in the non-CitSci corpus. The situation was opposite for climate change and its consequences on species distribution and adaptation, which was a central theme in the non-CitSci corpus only. We only revealed subtle differences in the relative importance of particular themes and in the way these themes are tackled in CitSci and non-CitSci articles, thus indicating that citizen science is well integrated in the main, classical research themes of ecology.

The co-existence of multiple oak leaf flushes contributes to the large within-tree variation in chemistry, insect attack and pathogen infection.

Many plant species produce multiple leaf flushes during the growing season, which might have major consequences for within-plant variation in chemistry and species interactions. Yet, we lack a theoretical or empirical framework for how differences among leaf flushes might shape variation in damage by insects and diseases. We assessed the impact of leaf flush identity on leaf chemistry, insect attack and pathogen infection on the pedunculate oak Quercus robur by sampling leaves from each leaf flush in 20 populations across seven European countries during an entire growing season. The first leaf flush had higher levels of primary compounds, and lower levels of secondary compounds, than the second flush, whereas plant chemistry was highly variable in the third flush. Insect attack decreased from the first to the third flush, whereas infection by oak powdery mildew was lowest on leaves from the first flush. The relationship between plant chemistry, insect attack and pathogen infection varied strongly among leaf flushes and seasons. Our findings demonstrate the importance of considering differences among leaf flushes for our understanding of within-tree variation in chemistry, insect attack and disease levels, something particularly relevant given the expected increase in the number of leaf flushes with climate change.

Recovery of moth and butterfly (Lepidoptera) communities in a polluted region following emission decline.

Environmental pollution is one of the major drivers of the present-day decline in global biodiversity. However, the links between the effects of industrial pollution on insect communities and the underlying species-specific responses remain poorly understood. We explored the spatial pattern in insect communities by analysing 581 samples of moths and butterflies (containing 25,628 individuals of 345 species) collected along a strong pollution gradient in subarctic Russia, and we recorded temporal changes in these communities during the pollution decline that occurred from 1992 to 2006. In the 1990s, the diversity of the Lepidoptera community was positively correlated with the distance from the copper-nickel smelter at Monchegorsk. The overall abundance of Lepidoptera did not change along the pollution gradient, although the abundance of many species decreased with increasing pollution. The responses of each individual species to pollution were associated with its life history traits. The abundances of monophagous species that fed inside live plant tissues and hibernated as imagoes or pupae were not affected by pollution, whereas the abundances of oligophagous and polyphagous species that fed externally on plants and hibernated as larvae generally declined near the smelter. Substantial decreases in aerial emissions from the smelter between 1992 and 2006 resulted in an increase in the diversity of moths and butterflies in severely polluted habitats, whereas their overall abundance did not change. This recovery of the Lepidoptera community occurred due to the reappearance of rare species that had been previously extirpated by pollution and was observed despite the lack of any signs of recovery of the vegetation in the heavily polluted sites. We conclude that the recovery trajectories of insect communities following emission control can be predicted from studies of their changes along spatial pollution gradients by using space-for-time substitution.

Herbivory on the pedunculate oak along an urbanization gradient in Europe: Effects of impervious surface, local tree cover, and insect feeding guild.

Urbanization is an important driver of the diversity and abundance of tree-associated insect herbivores, but its consequences for insect herbivory are poorly understood. A likely source of variability among studies is the insufficient consideration of intra-urban variability in forest cover. With the help of citizen scientists, we investigated the independent and interactive effects of local canopy cover and percentage of impervious surface on insect herbivory in the pedunculate oak (Quercus robur L.) throughout most of its geographic range in Europe. We found that the damage caused by chewing insect herbivores as well as the incidence of leaf-mining and gall-inducing herbivores consistently decreased with increasing impervious surface around focal oaks. Herbivory by chewing herbivores increased with increasing forest cover, regardless of impervious surface. In contrast, an increase in local canopy cover buffered the negative effect of impervious surface on leaf miners and strengthened its effect on gall inducers. These results show that-just like in non-urban areas-plant-herbivore interactions in cities are structured by a complex set of interacting factors. This highlights that local habitat characteristics within cities have the potential to attenuate or modify the effect of impervious surfaces on biotic interactions.

Changes in the foliar fungal community between oak leaf flushes along a latitudinal gradient in Europe.

Aim: Leaves support a large diversity of fungi, which are known to cause plant diseases, induce plant defences or influence leaf senescence and decomposition. To advance our understanding of how foliar fungal communities are structured and assembled, we assessed to what extent leaf flush and latitude can explain the within- and among-tree variation in foliar fungal communities. Location: A latitudinal gradient spanning c. 20 degrees in latitude in Europe. Taxa: The foliar fungal community associated with a foundation tree species, the pedunculate oak Quercus robur. Methods: We examined the main and interactive effects of leaf flush and latitude on the foliar fungal community by sampling 20 populations of the pedunculate oak Quercus robur across the tree's range. We used the ITS region as a target for characterization of fungal communities using DNA metabarcoding. Results: Species composition, but not species richness, differed between leaf flushes. Across the latitudinal gradient, species richness was highest in the central part of the oak's distributional range, and foliar fungal community composition shifted along the latitudinal gradient. Among fungal guilds, the relative abundance of plant pathogens and mycoparasites was lower on the first leaf flush, and the relative abundance of plant pathogens and saprotrophs decreased with latitude. Conclusions: Changes in community composition between leaf flushes and along the latitudinal gradient were mostly a result of species turnover. Overall, our findings demonstrate that leaf flush and latitude explain 5%-22% of the small- and large-scale spatial variation in the foliar fungal community on a foundation tree within the temperate region. Using space-for-time substitution, we expect that foliar fungal community structure will change with climate warming, with an increase in the abundance of plant pathogens and mycoparasites at higher latitudes, with major consequences for plant health, species interactions and ecosystem dynamics.

Combining phytochemicals and multitrophic interactions to control forest insect pests.

Forest pests can cause massive ecological and economic damage worldwide. Ecologically sound solutions to diminish forest insect pest impacts include the use of their natural enemies, such as predators and parasitoids, as well as entomopathogenic fungi, bacteria or viruses. Phytochemical compounds mediate most interactions between these organisms, but knowledge of such chemically mediated multitrophic relationships is still at its infancy for forest systems, particularly when compared to agricultural systems. Here, we highlight the main gaps in how phytochemicals of forest trees facilitate or interfere with trophic interactions between trees, insect herbivores, and interacting organisms including predators, parasitoids and microbes. We propose future avenues of research on phytochemical-based biocontrol of forest pests taking into account the characteristics of trees and forests.

Climate affects neighbour-induced changes in leaf chemical defences and tree diversity-herbivory relationships.

Associational resistance theory predicts that insect herbivory decreases with increasing tree diversity in forest ecosystems. However, the generality of this effect and its underlying mechanisms are still debated, particularly since evidence has accumulated that climate may influence the direction and strength of the relationship between diversity and herbivory.We quantified insect leaf herbivory and leaf chemical defences (phenolic compounds) of silver birch Betula pendula in pure and mixed plots with different tree species composition across 12 tree diversity experiments in different climates. We investigated whether the effects of neighbouring tree species diversity on insect herbivory in birch, that is, associational effects, were dependent on the climatic context, and whether neighbour-induced changes in birch chemical defences were involved in associational resistance to insect herbivory.We showed that herbivory on birch decreased with tree species richness (i.e. associational resistance) in colder environments but that this relationship faded as mean annual temperature increased.Birch leaf chemical defences increased with tree species richness but decreased with the phylogenetic distinctiveness of birch from its neighbours, particularly in warmer and more humid environments.Herbivory was negatively correlated with leaf chemical defences, particularly when birch was associated with closely related species. The interactive effect of tree diversity and climate on herbivory was partially mediated by changes in leaf chemical defences.Our findings confirm that tree species diversity can modify the leaf chemistry of a focal species, hence its quality for herbivores. They further stress that such neighbour-induced changes are dependent on climate and that tree diversity effects on insect herbivory are partially mediated by these neighbour-induced changes in chemical defences.

Effects of latitude and conspecific plant density on insect leaf herbivory in oak saplings and seedlings.

PREMISE: Abiotic factors and plant species traits have been shown to drive latitudinal gradients in herbivory, and yet, population-level factors have been largely overlooked within this context. One such factor is plant density, which may influence the strength of herbivory and may vary with latitude. METHODS: We measured insect herbivory and conspecific plant density (CPD) of oak (Quercus robur) seedlings and saplings along a 17° latitudinal gradient (2700 km) to test whether herbivory exhibited a latitudinal gradient, whether herbivory was associated with CPD, and whether such an association changed with latitude. RESULTS: We found a positive but saturating association between latitude and leaf herbivory. Furthermore, we found no significant relationship between CPD and herbivory, and such lack of density effects remained consistent throughout the sampled latitudinal gradient. CONCLUSIONS: Despite the apparently negligible influence of plant density on herbivory for Q. robur, further research with other plant taxa and in different types of plant communities are needed to investigate density-dependent processes shaping geographical variation in plant-herbivore interactions.

Tree Diversity and Forest Resistance to Insect Pests: Patterns, Mechanisms, and Prospects.

Ecological research conducted over the past five decades has shown that increasing tree species richness at forest stands can improve tree resistance to insect pest damage. However, the commonality of this finding is still under debate. In this review, we provide a quantitative assessment (i.e., a meta-analysis) of tree diversity effects on insect herbivory and discuss plausible mechanisms underlying the observed patterns. We provide recommendations and working hypotheses that can serve to lay the groundwork for research to come. Based on more than 600 study cases, our quantitative review indicates that insect herbivory was, on average, lower in mixed forest stands than in pure stands, but these diversity effects were contingent on herbivore diet breadth and tree species composition. In particular, tree species diversity mainly reduced damage of specialist insect herbivores in mixed stands with phylogenetically distant tree species. Overall, our findings provide essential guidance for forest pest management.

Leaf chemical defences and insect herbivory in oak: accounting for canopy position unravels marked genetic relatedness effects.

BACKGROUND AND AIMS: Highly controlled experiments document that plant genetic diversity and relatedness can shape herbivore communities and patterns of herbivory. Evidence from the field is, however, scarce and inconsistent. We assessed whether a genetic signal underlying herbivory can be detected in oak woodlands when accounting for variation at smaller (within-tree) and larger (among-stand) scales. METHODS: We tested relationships between tree genetic relatedness, leaf chemical defences and insect herbivory for different canopy layers in 240 trees from 15 pedunculate oak (Quercus robur) forest stands. We partitioned sources of variability in herbivory and defences among stands, individuals and branches. KEY RESULTS: Leaf defences, insect herbivory and their relationship differed systematically between the upper and the lower tree canopy. When accounting for this canopy effect, the variation explained by tree genetic relatedness rose from 2.8 to 34.1 % for herbivory and from 7.1 to 13.8 % for leaf defences. The effect was driven by markedly stronger relationships in the upper canopy. CONCLUSIONS: Our findings illustrate that considerable effects of the host plant genotype on levels of leaf chemical defences and associated insect herbivory can be detected in natural tree populations when within-individual variation is properly accounted for.

Latitudinal variation in seed predation correlates with latitudinal variation in seed defensive and nutritional traits in a widespread oak species.

BACKGROUND AND AIMS: Classic theory on geographical gradients in plant-herbivore interactions assumes that herbivore pressure and plant defences increase towards warmer and more stable climates found at lower latitudes. However, the generality of these expectations has been recently called into question by conflicting empirical evidence. One possible explanation for this ambiguity is that most studies have reported on patterns of either herbivory or plant defences whereas few have measured both, thus preventing a full understanding of the implications of observed patterns for plant-herbivore interactions. In addition, studies have typically not measured climatic factors affecting plant-herbivore interactions, despite their expected influence on plant and herbivore traits. METHODS: Here we tested for latitudinal variation in insect seed predation and seed traits putatively associated with insect attack across 36 Quercus robur populations distributed along a 20° latitudinal gradient. We then further investigated the associations between climatic factors, seed traits and seed predation to test for climate-based mechanisms of latitudinal variation in seed predation. KEY RESULTS: We found strong but contrasting latitudinal clines in seed predation and seed traits, whereby seed predation increased whereas seed phenolics and phosphorus decreased towards lower latitudes. We also found a strong direct association between temperature and seed predation, with the latter increasing towards warmer climates. In addition, temperature was negatively associated with seed traits, with populations at warmer sites having lower levels of total phenolics and phosphorus. In turn, these negative associations between temperature and seed traits led to a positive indirect association between temperature and seed predation. CONCLUSIONS: These results help unravel how plant-herbivore interactions play out along latitudinal gradients and expose the role of climate in driving these outcomes through its dual effects on plant defences and herbivores. Accordingly, this emphasizes the need to account for abiotic variation while testing concurrently for latitudinal variation in plant traits and herbivore pressure.

How do trees respond to species mixing in experimental compared to observational studies?

For decades, ecologists have investigated the effects of tree species diversity on tree productivity at different scales and with different approaches ranging from observational to experimental study designs. Using data from five European national forest inventories (16,773 plots), six tree species diversity experiments (584 plots), and six networks of comparative plots (169 plots), we tested whether tree species growth responses to species mixing are consistent and therefore transferrable between those different research approaches. Our results confirm the general positive effect of tree species mixing on species growth (16% on average) but we found no consistency in species-specific responses to mixing between any of the three approaches, even after restricting comparisons to only those plots that shared similar mixtures compositions and forest types. These findings highlight the necessity to consider results from different research approaches when selecting species mixtures that should maximize positive forest biodiversity and functioning relationships.

Responses of forest insect pests to climate change: not so simple.

Climate change is a multi-faceted phenomenon, including elevated CO2, warmer temperatures, more severe droughts and more frequent storms. All these components can affect forest pests directly, or indirectly through interactions with host trees and natural enemies. Most of the responses of forest insect herbivores to climate change are expected to be positive, with shorter generation time, higher fecundity and survival, leading to increased range expansion and outbreaks. Forest insect pest can also benefit from synergistic effects of several climate change pressures, such as hotter droughts or warmer storms. However, lesser known negative effects are also likely, such as lethal effects of heat waves or thermal shocks, less palatable host tissues or more abundant parasitoids and predators. The complex interplay between abiotic stressors, host trees, insect herbivores and their natural enemies makes it very difficult to predict overall consequences of climate change on forest health. This calls for the development of process-based models to simulate pest population dynamics under climate change scenarios.

Tree diversity drives associational resistance to herbivory at both forest edge and interior.

Tree diversity is increasingly acknowledged as an important driver of insect herbivory. However, there is still a debate about the direction of associational effects that can range from associational resistance (i.e., less damage in mixed stands than in monocultures) to the opposite, associational susceptibility. Discrepancies among published studies may be due to the overlooked effect of spatially dependent processes such as tree location within forests. We addressed this issue by measuring crown defoliation and leaf damage made by different guilds of insect herbivores on oaks growing among conspecific versus heterospecific neighbors at forest edges versus interior, in two closed sites in SW France forests. Overall, oaks were significantly less defoliated among heterospecific neighbors (i.e., associational resistance), at both forest edge and interior. At the leaf level, guild diversity and leaf miner herbivory significantly increased with tree diversity regardless of oak location within stands. Other guilds showed no clear response to tree diversity or oak location. We showed that herbivore response to tree diversity varied among insect feeding guilds but not between forest edges and interior, with inconsistent patterns between sites. Importantly, we show that oaks were more defoliated in pure oak plots than in mixed plots at both edge and forest interior and that, on average, defoliation decreased with increasing tree diversity from one to seven species. We conclude that edge conditions could be interacting with tree diversity to regulate insect defoliation, but future investigations are needed to integrate them into the management of temperate forests, notably by better understanding the role of the landscape context.

Greater phylogenetic distance from native oaks predicts escape from insect leaf herbivores by non-native oak saplings.

PREMISE: Non-native plant species have been hypothesized to experience lower herbivory in novel environments as a function of their phylogenetic distance from native plant species. Although recent work has found support for this prediction, the plant traits responsible for such patterns have been largely overlooked. METHODS: In a common garden experiment in northwestern Spain, we tested whether oak species (Quercus spp.) not native to this region that are phylogenetically more distantly related to native species exhibit less insect leaf herbivory. In addition, we also investigated plant traits potentially correlated with any such effect of phylogenetic distance. RESULTS: As expected, phylogenetic distance from native species negatively predicted insect leaf herbivory on non-native oaks. In addition, we found that the leaf traits, namely phosphorus and condensed tannins, were significantly associated with herbivory, suggesting that they are associated with the effect of phylogenetic distance on leaf herbivory on non-native oak species. CONCLUSIONS: This study contributes to a better understanding of how evolutionary relationships (relatedness) between native and non-native plant species determine the latter's success in novel environments via locally shared enemies, and encourages more work investigating the plant traits that mediate the effects of phylogenetic distance on enemy escape.

Biotic predictors complement models of bat and bird responses to climate and tree diversity in European forests.

Bats and birds are key providers of ecosystem services in forests. How climate and habitat jointly shape their communities is well studied, but whether biotic predictors from other trophic levels may improve bird and bat diversity models is less known, especially across large bioclimatic gradients. Here, we achieved multi-taxa surveys in 209 mature forests replicated in six European countries from Spain to Finland, to investigate the importance of biotic predictors (i.e. the abundance or activity of defoliating insects, spiders, earthworms and wild ungulates) for bat and bird taxonomic and functional diversity. We found that nine out of 12 bird and bat diversity metrics were best explained when biotic factors were added to models including climate and habitat variables, with a mean gain in explained variance of 38% for birds and 15% for bats. Tree functional diversity was the most important habitat predictor for birds, while bats responded more to understorey structure. The best biotic predictors for birds were spider abundance and defoliating insect activity, while only bat functional evenness responded positively to insect herbivory. Accounting for potential biotic interactions between bats, birds and other taxa of lower trophic levels will help to understand how environmental changes along large biogeographical gradients affect higher-level predator diversity in forest ecosystems.