Functional and phylogenetic relationships link predators to plant diversity via trophic and non-trophic pathways.

Human-induced biodiversity loss negatively affects ecosystem function, but the interactive effects of biodiversity change across trophic levels remain insufficiently understood. We sampled arboreal spiders and lepidopteran larvae across seasons in 2 years in a subtropical tree diversity experiment, and then disentangled the links between tree diversity and arthropod predator diversity by deconstructing the pathways among multiple components of diversity (taxonomic, phylogenetic and functional) with structural equation models. We found that herbivores were major mediators of plant species richness effects on abundance, species richness, functional and phylogenetic diversity of predators, while phylogenetic, functional and structural diversity of trees were also important mediators of this process. However, the strength and direction differed between functional, structural and phylogenetic diversity effects, indicating different underlying mechanisms for predator community assembly. Abundance and multiple diversity components of predators were consistently affected by tree functional diversity, indicating that the variation in structure and environment caused by plant functional composition might play key roles in predator community assembly. Our study highlights the importance of an integrated approach based on multiple biodiversity components in understanding the consequences of biodiversity loss in multitrophic communities.

Carbon-biodiversity relationships in a highly diverse subtropical forest.

Carbon-focused climate mitigation strategies are becoming increasingly important in forests. However, with ongoing biodiversity declines we require better knowledge of how much such strategies account for biodiversity. We particularly lack information across multiple trophic levels and on established forests, where the interplay between carbon stocks, stand age, and tree diversity might influence carbon-biodiversity relationships. Using a large dataset (>4600 heterotrophic species of 23 taxonomic groups) from secondary, subtropical forests, we tested how multitrophic diversity and diversity within trophic groups relate to aboveground, belowground, and total carbon stocks at different levels of tree species richness and stand age. Our study revealed that aboveground carbon, the key component of climate-based management, was largely unrelated to multitrophic diversity. By contrast, total carbon stocks-that is, including belowground carbon-emerged as a significant predictor of multitrophic diversity. Relationships were nonlinear and strongest for lower trophic levels, but nonsignificant for higher trophic level diversity. Tree species richness and stand age moderated these relationships, suggesting long-term regeneration of forests may be particularly effective in reconciling carbon and biodiversity targets. Our findings highlight that biodiversity benefits of climate-oriented management need to be evaluated carefully, and only maximizing aboveground carbon may fail to account for biodiversity conservation requirements.

Tree dissimilarity determines multi-dimensional beta-diversity of herbivores and carnivores via bottom-up effects.

Global biodiversity decline and its cascading effects through trophic interactions pose a severe threat to human society. Establishing the impacts of biodiversity decline requires a more thorough understanding of multi-trophic interactions and, more specifically, the effects that loss of diversity in primary producers has on multi-trophic community assembly. Within a synthetic conceptual framework for multi-trophic beta-diversity, we tested a series of hypotheses on neutral and niche-based bottom-up processes in assembling herbivore and carnivore communities in a subtropical forest using linear models, hieratical variance partitioning based on linear mixed-effects models (LMMs) and simulation. We found that the observed taxonomic, phylogenetic and functional beta-diversity of both herbivorous caterpillars and carnivorous spiders were significantly and positively related to tree dissimilarity. Linear models and variance partitioning for LMMs jointly suggested that as a result of bottom-up effects, producer dissimilarities were predominant in structuring consumer dissimilarity, the strength of which highly depended on the trophic dependencies on producers, the diversity facet examined, and data quality. Importantly, linear models for standardized beta-diversities against producer dissimilarities implied a transition between niche-based processes such as environmental filtering and competitive exclusion, which supports the role of bottom-up effect in determining consumer community assembly. These findings enrich our mechanistic understanding of the 'Diversity Begets Diversity' hypothesis and the complexity of higher-trophic community assembly, which is fundamental for sustainable biodiversity conservation and ecosystem management.

Tree communities and functional traits determine herbivore compositional turnover.

There are many factors known to drive species turnover, although the mechanisms by which these operate are less clear. Based on comprehensive datasets from the largest tree diversity experiment worldwide (BEF-China), we used shared herbivore species (zeta diversity) and multi-site generalized dissimilarity modelling to investigate the patterns and determinants of species turnover of Lepidoptera herbivores among study plots across a gradient in tree species richness. We found that zeta diversity declined sharply with an increasing number of study plots, with complete changes in caterpillar species composition observed even at the fine spatial scale of our study. Plant community characteristics rather than abiotic factors were found to play key roles in driving caterpillar compositional turnover, although these effects varied with an increasing number of study plots considered, due to the varying contributions of rare and common species to compositional turnover. Our study reveals details of the impact of phylogeny- and trait-mediated processes of trees on herbivore compositional turnover, which has implications for forest management and conservation and shows potential avenues for maintenance of heterogeneity in herbivore communities.

Tree species richness modulates water supply in the local tree neighbourhood: evidence from wood δ13C signatures in a large-scale forest experiment.

Biodiversity is considered to mitigate the adverse effects of changing precipitation patterns. However, our understanding of how tree diversity at the local neighbourhood scale modulates the water use and leaf physiology of individual trees remains unclear. We made use of a large-scale tree diversity experiment in subtropical China to study eight tree species along an experimentally manipulated gradient of local neighbourhood tree species richness. Twig wood carbon isotope composition (δ13Cwood) was used as an indicator for immediate leaf-level responses to water availability in relation to local neighbourhood conditions and a target tree's functional traits. Across species, a target tree's δ13Cwood signatures decreased progressively with increasing neighbourhood species richness, with effects being strongest at high neighbourhood shading intensity. Moreover, the δ13Cwood-shading relationship shifted from positive (thin-leaved species) or neutral (thick-leaved species) in conspecific to negative in heterospecific neighbourhoods, most likely owing to a lower interspecific competition for water and microclimate amelioration. This suggests that promoting tree species richness at the local neighbourhood scale may improve a tree's local water supply with potential effects for an optimized water-use efficiency of tree communities during drought. This assumption, however, requires validation by further studies that focus on mechanisms that regulate the water availability in mixtures.

Genetic richness affects trait variation but not community productivity in a tree diversity experiment.

Biodiversity-ecosystem functioning experiments found that productivity generally increases with species richness, but less is known about effects of within-species genetic richness and potential interactions between the two. While functional differences between species can explain species richness effects, empirical evidence regarding functional differences between genotypes within species and potential consequences for productivity is largely lacking. We therefore measured within- and among-species variation in functional traits and growth and determined stand-level tree biomass in a large forest experiment factorially manipulating species and genetic richness in subtropical China. Within-species variation across genetic seed families, in addition to variation across species, explained a substantial amount of trait variation. Furthermore, trait responses to species and genetic richness varied significantly within and between species. Multivariate trait variation was larger among individuals from species mixtures than those from species monocultures, but similar among individuals from genetically diverse vs genetically uniform monocultures. Correspondingly, species but not genetic richness had a positive effect on stand-level tree biomass. We argue that identifying functional diversity within and among species in forest communities is necessary to separate effects of species and genetic diversity on tree growth and community productivity.

Host functional and phylogenetic composition rather than host diversity structure plant-herbivore networks.

Declining plant diversity alters ecological networks, such as plant-herbivore interactions. However, our knowledge of the potential mechanisms underlying effects of plant species loss on plant-herbivore network structure is still limited. We used DNA barcoding to identify herbivore-host plant associations along declining levels of tree diversity in a large-scale, subtropical biodiversity experiment. We tested for effects of tree species richness, host functional and phylogenetic diversity, and host functional (leaf trait) and phylogenetic composition on species, phylogenetic and network composition of herbivore communities. We found that phylogenetic host composition and related palatability/defence traits but not tree species richness significantly affected herbivore communities and interaction network complexity at both the species and community levels. Our study indicates that evolutionary dependencies and functional traits of host plants determine the composition of higher trophic levels and corresponding interaction networks in species-rich ecosystems. Our findings highlight that characteristics of the species lost have effects on ecosystem structure and functioning across trophic levels that cannot be predicted from mere reductions in species richness.

Neighbour species richness and local structural variability modulate aboveground allocation patterns and crown morphology of individual trees.

Local neighbourhood interactions are considered a main driver for biodiversity-productivity relationships in forests. Yet, the structural responses of individual trees in species mixtures and their relation to crown complementarity remain poorly understood. Using a large-scale forest experiment, we studied the impact of local tree species richness and structural variability on above-ground wood volume allocation patterns and crown morphology. We applied terrestrial laser scanning to capture the three-dimensional structure of trees and their temporal dynamics. We found that crown complementarity and crown plasticity increased with species richness. Trees growing in species-rich neighbourhoods showed enhanced aboveground wood volume both in trunks and branches. Over time, neighbourhood diversity induced shifts in wood volume allocation in favour of branches, in particular for morphologically flexible species. Our results demonstrate that diversity-mediated shifts in allocation pattern and crown morphology are a fundamental mechanism for crown complementarity and may be an important driver of overyielding.

Tree diversity increases robustness of multi-trophic interactions.

Multi-trophic interactions maintain critical ecosystem functions. Biodiversity is declining globally, while responses of trophic interactions to biodiversity change are largely unclear. Thus, studying responses of multi-trophic interaction robustness to biodiversity change is crucial for understanding ecosystem functioning and persistence. We investigate plant-Hemiptera (antagonism) and Hemiptera-ant (mutualism) interaction networks in response to experimental manipulation of tree diversity. We show increased diversity at both higher trophic levels (Hemiptera and ants) and increased robustness through redundancy of lower level species of multi-trophic interactions when tree diversity increased. Hemiptera and ant diversity increased with tree diversity through non-additive diversity effects. Network analyses identified that tree diversity also increased the number of tree and Hemiptera species used by Hemiptera and ant species, and decreased the specialization on lower trophic level species in both mutualistic and antagonist interactions. Our results demonstrate that bottom-up effects of tree diversity ascend through trophic levels regardless of interaction type. Thus, local tree diversity is a key driver of multi-trophic community diversity and interaction robustness in forests.

Tree-species interactions increase light absorption and growth in Chinese subtropical mixed-species plantations.

Light-related interactions can increase productivity in tree-species mixtures compared with monocultures due to higher stand-level absorption of photosynthetically active radiation (APAR) or light-use efficiency (LUE). However, the effects of different light-related interactions, and their relative importance, have rarely been quantified. Here, measurements of vertical leaf-area distributions, tree sizes, and stand density were combined with a tree-level light model (Maestra) to examine how crown architecture and vertical or horizontal canopy structure influence the APAR of 16 monocultures and eight different two-species mixtures with 16 different species in a Chinese subtropical tree diversity experiment. A higher proportion of crown leaf area occurred in the upper crowns of species with higher specific leaf areas. Tree-level APAR depended largely on tree leaf area and also, but to a lesser extent, on relative height (i.e., tree dominance) and leaf-area index (LAI). Stand-level APAR depended on LAI and canopy volume, but not on the vertical stratification or canopy leaf-area density. The mixing effects, in terms of relative differences between mixtures and monocultures, on stand-level APAR were correlated with the mixing effects on basal area growth, indicating that light-related interactions may have been responsible for part of the mixing effects on basal area growth. While species identity influences the vertical distributions of leaf area within tree crowns, this can have a relatively small effect on tree and stand APAR compared with the size and vertical positioning of the crowns, or the LAI and canopy volume.

Tree species richness increases ecosystem carbon storage in subtropical forests.

Forest ecosystems are an integral component of the global carbon cycle as they take up and release large amounts of C over short time periods (C flux) or accumulate it over longer time periods (C stock). However, there remains uncertainty about whether and in which direction C fluxes and in particular C stocks may differ between forests of high versus low species richness. Based on a comprehensive dataset derived from field-based measurements, we tested the effect of species richness (3-20 tree species) and stand age (22-116 years) on six compartments of above- and below-ground C stocks and four components of C fluxes in subtropical forests in southeast China. Across forest stands, total C stock was 149 ± 12 Mg ha-1 with richness explaining 28.5% and age explaining 29.4% of variation in this measure. Species-rich stands had higher C stocks and fluxes than stands with low richness; and, in addition, old stands had higher C stocks than young ones. Overall, for each additional tree species, the total C stock increased by 6.4%. Our results provide comprehensive evidence for diversity-mediated above- and below-ground C sequestration in species-rich subtropical forests in southeast China. Therefore, afforestation policies in this region and elsewhere should consider a change from the current focus on monocultures to multi-species plantations to increase C fixation and thus slow increasing atmospheric CO2 concentrations and global warming.

From competition to facilitation: how tree species respond to neighbourhood diversity.

Studies on tree communities have demonstrated that species diversity can enhance forest productivity, but the driving mechanisms at the local neighbourhood level remain poorly understood. Here, we use data from a large-scale biodiversity experiment with 24 subtropical tree species to show that neighbourhood tree species richness generally promotes individual tree productivity. We found that the underlying mechanisms depend on a focal tree's functional traits: For species with a conservative resource-use strategy diversity effects were brought about by facilitation, and for species with acquisitive traits by competitive reduction. Moreover, positive diversity effects were strongest under low competition intensity (quantified as the total basal area of neighbours) for acquisitive species, and under high competition intensity for conservative species. Our findings demonstrate that net biodiversity effects in tree communities can vary over small spatial scales, emphasising the need to consider variation in local neighbourhood interactions to better understand effects at the community level.

Ants at Plant Wounds: A Little-Known Trophic Interaction with Evolutionary Implications for Ant-Plant Interactions.

Extrafloral nectaries (EFNs) allow plants to engage in mutualisms with ants, preventing herbivory in exchange for food. EFNs occur scattered throughout the plant phylogeny and likely evolved independent from herbivore-created wounds subsequently visited by ants collecting leaked sap. Records of wound-feeding ants are, however, anecdotal. By surveying 38,000 trees from 40 species, we conducted the first quantitative ecological study of this overlooked behavior. Ant-wound interactions were widespread (0.5% of tree individuals) and occurred on 23 tree species. Interaction networks were opportunistic, closely resembling ant-EFN networks. Fagaceae, a family lacking EFNs, was strongly overrepresented. For Fagaceae, ant occurrence at wounds correlated with species-level leaf damage, potentially indicating that wounds may attract mutualistic ants, which supports the hypothesis of ant-tended wounds as precursors of ant-EFN mutualisms. Given that herbivore wounds are common, wound sap as a steadily available food source might further help to explain the overwhelming abundance of ants in (sub)tropical forest canopies.

Tree species richness attenuates the positive relationship between mutualistic ant-hemipteran interactions and leaf chewer herbivory.

Interactions across trophic levels influence plant diversity effects on ecosystem functions, but the complexity of these interactions remains poorly explored. For example, the interplay between different interactions (e.g. mutualism, predation) might be an important moderator of biodiversity-ecosystem function relationships. We tested for relationships between trophobioses (facultative ant-hemipteran mutualism) and leaf chewer herbivory in a subtropical forest biodiversity experiment. We analysed trophobiosis and herbivory data of more than 10 000 trees along a tree species richness gradient. Against expectations, chewing damage was higher on trees with trophobioses. However, the net positive relationship between trophobioses and overall herbivory depended on tree species richness, being most pronounced at low richness. Our results point to indirect, positive effects of ant-tended sap suckers on leaf chewers, potentially by altering plant defences. Direct antagonistic relationships of trophobiotic ants and leaf-chewing herbivores-frequently reported to drive community-wide effects of trophobioses in other ecosystems-seemed less relevant. However, antagonistic interactions likely contributed to the attenuating effect of tree species richness, because trophobiotic ant and herbivore communities changed from monocultures to species-rich mixtures. Our findings, therefore, suggest that biodiversity loss might lead to complex changes in higher trophic level effects on ecosystem functions, mediated by both trophic and non-trophic interactions.

Functional and phylogenetic diversity of woody plants drive herbivory in a highly diverse forest.

Biodiversity loss may alter ecosystem processes, such as herbivory, a key driver of ecological functions in species-rich (sub)tropical forests. However, the mechanisms underlying such biodiversity effects remain poorly explored, as mostly effects of species richness - a very basic biodiversity measure - have been studied. Here, we analyze to what extent the functional and phylogenetic diversity of woody plant communities affect herbivory along a diversity gradient in a subtropical forest. We assessed the relative effects of morphological and chemical leaf traits and of plant phylogenetic diversity on individual-level variation in herbivory of dominant woody plant species across 27 forest stands in south-east China. Individual-level variation in herbivory was best explained by multivariate, community-level diversity of leaf chemical traits, in combination with community-weighted means of single traits and species-specific phylodiversity measures. These findings deviate from those based solely on trait variation within individual species. Our results indicate a strong impact of generalist herbivores and highlight the need to assess food-web specialization to determine the direction of biodiversity effects. With increasing plant species loss, but particularly with the concomitant loss of functional and phylogenetic diversity in these forests, the impact of herbivores will probably decrease - with consequences for the herbivore-mediated regulation of ecosystem functions.

The spatial distribution of tree-tree interaction effects on soil microbial biomass and respiration.

The capacity of forests to sequester carbon in both above- and belowground compartments is a crucial tool to mitigate rising atmospheric carbon concentrations. Belowground carbon storage in forests is strongly linked to soil microbial communities that are the key drivers of soil heterotrophic respiration, organic matter decomposition and thus nutrient cycling. However, the relationships between tree diversity and soil microbial properties such as biomass and respiration remain unclear with inconsistent findings among studies. It is unknown so far how the spatial configuration and soil depth affect the relationship between tree richness and microbial properties. Here, we studied the spatial distribution of soil microbial properties in the context of a tree diversity experiment by measuring soil microbial biomass and respiration in subtropical forests (BEF-China experiment). We sampled soil cores at two depths at five locations along a spatial transect between the trees in mono- and hetero-specific tree pairs of the native deciduous species Liquidambar formosana and Sapindus saponaria. Our analyses showed decreasing soil microbial biomass and respiration with increasing soil depth and distance from the tree in mono-specific tree pairs. We calculated belowground overyielding of soil microbial biomass and respiration - which is higher microbial biomass or respiration than expected from the monocultures - and analysed the distribution patterns along the transect. We found no general overyielding across all sampling positions and depths. Yet, we encountered a spatial pattern of microbial overyielding with a significant microbial overyielding close to L. formosana trees and microbial underyielding close to S. saponaria trees. We found similar spatial patterns across microbial properties and depths that only differed in the strength of their effects. Our results highlight the importance of small-scale variations of tree-tree interaction effects on soil microbial communities and functions and are calling for better integration of within-plot variability to understand biodiversity-ecosystem functioning relationships.

Tree and shrub richness modifies subtropical tree productivity by regulating the diversity and community composition of soil bacteria and archaea.

BACKGROUND: Declines in plant biodiversity often have negative consequences for plant community productivity, and it becomes increasingly acknowledged that this may be driven by shifts in soil microbial communities. So far, the role of fungal communities in driving tree diversity-productivity relationships has been well assessed in forests. However, the role of bacteria and archaea, which are also highly abundant in forest soils and perform pivotal ecosystem functions, has been less investigated in this context. Here, we investigated how tree and shrub richness affects stand-level tree productivity by regulating bacterial and archaeal community diversity and composition. We used a landscape-scale, subtropical tree biodiversity experiment (BEF-China) where tree (1, 2, or 4 species) and shrub richness (0, 2, 4, 8 species) were modified. RESULTS: Our findings indicated a noteworthy decline in soil bacterial α-diversity as tree species richness increased from monoculture to 2- and 4- tree species mixtures, but a significant increase in archaeal α-diversity. Additionally, we observed that the impact of shrub species richness on microbial α-diversity was largely dependent on the level of tree species richness. The increase in tree species richness greatly reduced the variability in bacterial community composition and the complexity of co-occurrence network, but this effect was marginal for archaea. Both tree and shrub species richness increased the stand-level tree productivity by regulating the diversity and composition of bacterial community and archaeal diversity, with the effects being mediated via increases in soil C:N ratios. CONCLUSIONS: Our findings provide insight into the importance of bacterial and archaeal communities in driving the relationship between plant diversity and productivity in subtropical forests and highlight the necessity for a better understanding of prokaryotic communities in forest soils. Video Abstract.

Effects of enemy exclusion on biodiversity-productivity relationships in a subtropical forest experiment.

Interspecific niche complementarity is a key mechanism posited to explain positive species richness-productivity relationships in plant communities. However, the exact nature of the niche dimensions that plant species partition remains poorly known.Species may partition abiotic resources that limit their growth, but species may also be specialized with respect to their set of biotic interactions with other trophic levels, in particular with enemies including pathogens and consumers. The lower host densities present in more species-diverse plant communities may therefore result in smaller populations of specialized enemies, and in a smaller associated negative feedback these enemies exert on plant productivity.To test whether such host density-dependent effects of enemies drive diversity-productivity relationships in young forest stands, we experimentally manipulated leaf fungal pathogens and insect herbivores in a large subtropical forest biodiversity-ecosystem functioning experiment in China (BEF-China).We found that fungicide spraying of tree canopies removed the positive tree-species richness-productivity relationship present in untreated control plots. The tree species that contributed the most to this effect were the ones with the highest fungicide-induced growth increase in monoculture. Insecticide application did not cause comparable effects. Synthesis. Our findings suggest that tree species diversity may not only promote productivity by interspecific resource-niche partitioning but also by trophic niche partitioning. Most likely, partitioning occurred with respect to enemies such as pathogenic fungi. Alternatively, similar effects on tree growth would have occurred if fungicide had eliminated positive effects of a higher diversity of beneficial fungi (e.g. mycorrhizal symbionts) that may have occurred in mixed tree species communities.

Local Tree Diversity Suppresses Foliar Fungal Infestation and Decreases Morphological But Not Molecular Richness in a Young Subtropical Forest.

Leaf fungal pathogens alter their host species' performance and, thus, changes in fungal species composition can translate into effects at the tree community scale. Conversely, the functional diversity of tree species in a host tree's local neighbourhood can affect the host's foliar fungal infestation. Therefore, understanding the factors that affect fungal infestations is important to advance our understanding of biodiversity-ecosystem functioning (BEF) relationships. Here we make use of the largest BEF tree experiment worldwide, the BEF-China experiment, where we selected tree host species with different neighbour species. Identifying fungal taxa by microscopy and by high-throughput DNA sequencing techniques based on the internal transcribed spacer (ITS) rDNA region, we analysed the fungal richness and infestation rates of our target trees as a function of local species richness. Based on the visual microscopic assessment, we found that a higher tree diversity reduced fungal richness and host-specific fungal infestation in the host's local neighbourhood, while molecular fungal richness was unaffected. This diversity effect was mainly explained by the decrease in host proportion. Thus, the dilution of host species in the local neighbourhood was the primary mechanism in reducing the fungal disease severity. Overall, our study suggests that diverse forests will suffer less from foliar fungal diseases compared to those with lower diversity.

What shapes ground beetle assemblages in a tree species-rich subtropical forest?

As woody plants provide much of the trophic basis for food webs in forests their species richness, but also stand age and numerous further variables such as vegetation structure, soil properties and elevation can shape assemblages of ground beetles (Coleoptera: Carabidae). However, the combined impact of these numerous variables on ground beetle diversity and community structure has rarely been studied simultaneously. Therefore, ground beetles were studied in 27 plots in a highly diverse and structurally heterogeneous subtropical forest ecosystem, the Gutianshan National Park (southeast China) using pitfall traps and flight interception traps. Both trapping methods collected partly overlapping species spectra. The arboreal fauna was dominated by lebiines and to a smaller extent by tiger beetles and platynines; the epigeic fauna comprised mostly representatives of the genus Carabus and numerous tribes, especially anisodactylines, pterostichines, and sphodrines. Ground beetle species richness, abundance, and biomass of the pitfall trap catches were analyzed with generalized linear mixed models (GLMMs), fitted with seven environmental variables. Four of these variables influenced the ground beetle assemblages: Canopy cover, herb cover, pH-value of the topsoil and elevation. Contrary to our expectations, woody plant species richness and stand age did not significantly affect ground beetle assemblages. Thus, ground beetles seem to respond differently to environmental variables than ants and spiders, two other predominantly predatory arthropod groups that were studied on the same plots in our study area and which showed distinct relationships with woody plant richness. Our results highlight the need to study a wider range of taxa to achieve a better understanding of how environmental changes affect species assemblages and their functioning in forest ecosystems.