Increased diversity by cushion plants enhances alpine community productivity and stability.

Biodiversity effects on ecosystem functioning in a 15-year grassland experiment: Patterns, mechanisms, and open questions

SummaryPlant community productivity commonly increases with increasing plant diversity, which is explained by complementarity among plant species in resource utilization (complementarity effect), or by selection of particularly productive plant species in diverse plant communities (selection effect). Recent studies have also shown that soil biota can drive the positive plant diversity–productivity relationship by suppressing productivity more in low‐ than in high‐diversity plant communities. However, much remains unknown about whether soil fertility plays a role in determining how soil biota affect plant diversity–productivity relationships.We hypothesized that under high soil fertility conditions, negative soil biota effects dominate, which reduces plant monoculture biomass more than that of high‐diversity plant communities. Conversely, under low soil fertility conditions, we hypothesized positive soil biota effects dominate, which facilitates plant resource partitioning and enhances community‐level biomass in high‐diversity plant communities. Hence, we expected positive plant diversity–community productivity relationships under low and high soil fertility conditions but caused by different mechanisms.We tested these hypotheses using woody seedlings and set up plant assemblages with four species richness levels (one, two, four and eight species), and grew them in sterilized and unsterilized (sterilized soil + living soil inoculum) soils at two nutrient levels (low versus high fertility).We found that at high fertility negative soil biota effects dominated and suppressed plant community biomass more in high‐diversity plant communities than in monocultures, resulting in reduced complementarity effects of diverse plant communities and a non‐significant plant species richness–community biomass relationship in unsterilized soil. Whereas at low fertility soil biota had net neutral to positive effects on plant community biomass but the beneficial effects did not increase with increasing plant species richness. Instead, soil biota neutrally affected the positive plant species richness–community biomass relationship, presumably due to non‐specific effects of beneficial soil biota.Synthesis. Soil biota and soil fertility interactively determine plant species richness–community biomass relationships. Moreover, soil biota modulate the complementary resource use among plant species. These findings suggest that environmental context plays an important role in determining whether and how soil biota generate the biodiversity–productivity relationship. Future studies would benefit from revealing the mechanisms underlying the interactive effects of soil biota, soil fertility, and plant diversity on ecosystem functioning.

Plants respond to herbivore attack by emitting a blend of volatiles called herbivore-induced plant volatiles (HIPVs), which attract arthropod natural enemies. Under natural conditions and multiple cropping agriculture systems, natural enemies are thought to encounter a mixture of HIPVs emanating from multiple plant species. The effect of such a mixture of HIPVs on the responses of natural enemies under field conditions has not been explored. Our study assessed whether a mixture of HIPVs from multiple host plant species influenced predator responses in field-cage conditions. We investigated (1) foraging behaviors of a predatory bug, Orius strigicollis, on cotton bollworm (Helicoverpa armigera) larvae-infested multiple host plant species, and (2) the attractiveness of a mixture of reconstituted HIPVs from multiple plant species to O. strigicollis in outdoor cages. Significantly, greater numbers of predators were attracted to H. armigera-infested multiple plant species. The predators exterminated significantly greater numbers of H. armigera larvae with the multiple versus single plant species treatments. Significantly, greater numbers of O. strigicollis were captured on traps baited with the mixture of reconstituted HIPVs from multiple versus single plant species. The enhanced attractiveness of a mixture of HIPVs from multiple plant species to O. strigicollis might be the result of an additive effect of HIPVs from the three plant species when combined in a mixture.

Summary1. Recent theoretical studies suggest that the stability of ecosystem processes is not governed by diversityper se, but by multitrophic interactions in complex communities. However, experimental evidence supporting this assumption is scarce.2. We investigated the impact of plant diversity and the presence of above‐ and below‐ground invertebrates on the stability of plant community productivity in space and time, as well as the interrelationship between both stability measures in experimental grassland communities.3. We sampled above‐ground plant biomass on subplots with manipulated above‐ and below‐ground invertebrate densities of a grassland biodiversity experiment (Jena Experiment) 1, 4 and 6 years after the establishment of the treatments to investigate temporal stability. Moreover, we harvested spatial replicates at the last sampling date to explore spatial stability.4. The coefficient of variation of spatial and temporal replicates served as a proxy for ecosystem stability. Both spatial and temporal stability increased to a similar extent with plant diversity. Moreover, there was a positive correlation between spatial and temporal stability, and elevated plant density might be a crucial factor governing the stability of diverse plant communities.5. Above‐ground insects generally increased temporal stability, whereas impacts of both earthworms and above‐ground insects depended on plant species richness and the presence of grasses. These results suggest that inconsistent results of previous studies on the diversity–stability relationship have in part been due to neglecting higher trophic‐level interactions governing ecosystem stability.6. Changes in plant species diversity in one trophic level are thus unlikely to mirror changes in multitrophic interrelationships. Our results suggest that both above‐ and below‐ground invertebrates decouple the relationship between spatial and temporal stability of plant community productivity by differently affecting the homogenizing mechanisms of plants in diverse plant communities.7.Synthesis. Species extinctions and accompanying changes in multitrophic interactions are likely to result not only in alterations in the magnitude of ecosystem functions but also in its variability complicating the assessment and prediction of consequences of current biodiversity loss.

Although the positive effects of biodiversity on ecosystem functioning and stability have been extensively documented in the literature, previous studies have mostly explored the mechanisms of functioning and stability independently. It is unclear how biodiversity effects on functioning may covary with those on stability. Here we developed an integrated framework to explore links between mechanisms underlying biodiversity effects on functioning and those on stability. Specifically, biodiversity effects on ecosystem functioning were partitioned into complementarity effects (CE) and selection effects (SE), and those on stability were partitioned into species asynchrony and species stability. We investigated how CE and SE were linked to species asynchrony and stability and how their links might be mediated by species evenness, using a multi‐site grassland experiment. Our mixed‐effects models showed that a higher community productivity was mainly due to CE and a higher community stability was mainly due to species asynchrony. Moreover, CE was positively related to species asynchrony, thus leading to a positive association between ecosystem productivity and stability. We used a structural equation model to illustrate how species evenness might mediate links between the various mechanisms. Communities with a higher evenness exhibited a higher CE and species asynchrony, but a lower SE and species stability. These evenness‐mediated associations enhanced the positive relationship between CE and species asynchrony, but blurred that between SE and species asynchrony. Synthesis. Our findings demonstrate mechanistic links between biodiversity effects on ecosystem functioning and stability. By doing so, our study contributes a novel framework for understanding ecological mechanisms of the functioning–stability relationship, which has important implications for developing management plans focused on strengthening synergies between ecosystem functioning and stability over the long term.

Theoretical studies of the relationship between ecosystem complexity and stability usually conclude that systems with more species, more interspecific interactions per species (connectance), or stronger interactions are not as likely to be stable as systems with fewer of these attributes (Gardner and Ashby 1970; May 1972, 1974, 1979; DeAngelis 1975; Gilpin 1975; Pimm 1979a, 1979b, 1980). Yet, in one of the few empirical investigations of this problem, McNaughton (1977) concluded that increased complexity stabilized certain ecosystem properties; more precisely, that a large mammalian grazer changed total green plant biomass less in more diverse than in less diverse grassland plots. We try to resolve this apparent contradiction between theory and empiricism by investigating, in model grazing systems, the relationship between complexity and the lack of change in plant biomass (which we call biomass stability) following the removal of an herbivore. We established a set of structured food web models composed of one herbivore and n plant species. The models were based on the familiar Lotka-Volterra equations, and we selected their parameters over intervals designed to be biologically sensible and also to reflect the pattern of interactions in the food web. Only those models with a locally stable equilibrium involving species with positive biomasses were retained for further analysis. From each model of this subset, the herbivore was removed and the resultant change in total plant biomass followed until a new stable equilibrium was achieved. Relative biomass stability was calculated from the relative change in the total plant biomasses of the two equilibria. Clearly, a ratio near unity indicates biomass stability, while a large ratio indicates that biomass has increased considerably, following removal of the herbivore. We modeled webs of varying complexity as measured by: (1) the number of species; (2) the number of competitive interactions between plant species; and (3) species diversity (a measure combining the number of species and their relative abundances), and related these features to biomass stability. Our conclusion is that increased complexity can enhance biomass stability, even

Summary 1. There is general concern that local loss of plant diversity will adversely impact net primary productivity and other ecosystem properties. However, mechanisms linking plant diversity with other trophic levels, especially for large herbivores, are poorly understood. 2. We examine the responses of foraging sheep to changes in plant species richness in an indoor cafeteria experiment involving six plant species richness levels (1, 2, 4, 6, 8 and 11 species) and three plant functional group compositions within each level, and in a field experiment involving three plant species richness levels (1, 4–6 or >8 species). 3. Sheep preferred a diverse diet over a single diet even when palatable species were in the diet. Voluntary daily intake steadily rose with increases in plant species richness in both cafeteria and field experiments. The overall nutrient intake (i.e. daily energy and protein intakes) of sheep in the cafeteria also rose significantly with increased plant species richness until it reached a plateau at eight species. The quality of the diet selected by sheep was also significantly affected by plant species richness, but the variation of dietary quality was small and variable. 4. High nutrient acquisition by the sheep depended on selecting those palatable species with high nutrient content from the plant forage on offer together with the complementary effects of plant species richness, especially for plant functional group richness. 5. Synthesis and applications. Our experiments demonstrate an asymptotic relationship between plant species richness and voluntary intake by sheep. Increases in plant species richness from a low level led to increased daily nutrient intake, and presumably performance of the sheep. Natural grasslands are generally low in nutritional quality and so plant species richness will critically influence herbivore food intake and nutrition. The asymptotic relationship indicates that the maintenance of plant species richness in rangelands will benefit both domestic herbivore production and the conservation of biodiversity.

Plant diversity effects on arthropods and arthropod-dependent ecosystem functions in a biodiversity experiment

Abstract. Modern grassland management seeks to provide many ecosystem services and experimental studies in resource-poor grasslands have shown a positive relationship between plant species richness and a variety of ecosystem functions. Thus, increasing species richness might help to enhance multifunctionality in managed grasslands if the relationship between species richness and ecosystem functioning is equally valid in high-input grassland systems. We tested the relative effects of low-input to high-input management intensities and low to high plant species richness. Using a combination of mowing frequencies (1, 2 or 4 cuts per season) and fertilisation levels (0, 100 and 200 kg N ha−1 a−1), we studied the productivity of 78 experimental grassland communities of increasing plant species richness (1, 2, 4, 8 or 16 species with 1 to 4 functional groups) in two successive years. Our results showed that in both years higher diversity was more effective in increasing productivity than higher management intensity: the 16-species mixtures had a surplus of 449 g m−2 y−1 in 2006 and 492 g m−2 y−1 in 2007 over the monoculture yields whereas the high-input management resulted in only 315 g m−2 y−1 higher productivity in 2006 and 440 g m−2 y−1 in 2007 than the low-input management. In addition, high-diversity low-input grassland communities had similar productivity as low-diversity high-input communities. The slopes of the biodiversity – productivity relationships significantly increased with increasing levels of management intensity in both years. We conclude that the biological mechanisms leading to enhanced biomass production in diverse grassland communities are as effective for productivity as a combination of several agricultural measures. Our results demonstrate that high-diversity low-input grassland communities provide not only a high diversity of plants and other organisms, but also ensure high forage yields, thus granting the basis for multifunctional managed grasslands.

Summary Hundreds of experiments have now manipulated species richness (SR) of various groups of organisms and examined how this aspect of biological diversity influences ecosystem functioning. Ecologists have recently expanded this field to look at whether phylogenetic diversity (PD) among species, often quantified as the sum of branch lengths on a molecular phylogeny leading to all species in a community, also predicts ecological function. Some have hypothesized that phylogenetic divergence should be a superior predictor of ecological function than SR because evolutionary relatedness represents the degree of ecological and functional differentiation among species. But studies to date have provided mixed support for this hypothesis. Here, we reanalyse data from 16 experiments that have manipulated plant SR in grassland ecosystems and examined the impact on above‐ground biomass production over multiple time points. Using a new molecular phylogeny of the plant species used in these experiments, we quantified how the PD of plants impacts average community biomass production as well as the stability of community biomass production through time. Using four complementary analyses, we show that, after statistically controlling for variation in SR, PD (the sum of branches in a molecular phylogenetic tree connecting all species in a community) is neither related to mean community biomass nor to the temporal stability of biomass. These results run counter to past claims. However, after controlling for SR, PD was positively related to variation in community biomass over time due to an increase in the variances of individual species, but this relationship was not strong enough to influence community stability. In contrast to the non‐significant relationships between PD, biomass and stability, our analyses show that SR per se tends to increase the mean biomass production of plant communities, after controlling for PD. The relationship between SR and temporal variation in community biomass was either positive, non‐significant or negative depending on which analysis was used. However, the increases in community biomass with SR, independently of PD, always led to increased stability. These results suggest that PD is no better as a predictor of ecosystem functioning than SR. Synthesis. Our study on grasslands offers a cautionary tale when trying to relate PD to ecosystem functioning suggesting that there may be ecologically important trait and functional variation among species that is not explained by phylogenetic relatedness. Our results fail to support the hypothesis that the conservation of evolutionarily distinct species would be more effective than the conservation of SR as a way to maintain productive and stable communities under changing environmental conditions.

Changes in producer diversity cause multiple changes in consumer communities through various mechanisms. However, past analyses investigating the relationship between plant diversity and arthropod consumers focused only on few aspects of arthropod diversity, e.g. species richness and abundance. Yet, shifts in understudied facets of arthropod diversity like relative abundances or species dominance may have strong effects on arthropod-mediated ecosystem functions. Here we analyze the relationship between plant species richness and arthropod diversity using four complementary diversity indices, namely: abundance, species richness, evenness (equitability of the abundance distribution) and dominance (relative abundance of the dominant species). Along an experimental gradient of plant species richness (1, 2, 4, 8, 16 and 60 plant species), we sampled herbivorous and carnivorous arthropods using pitfall traps and suction sampling during a whole vegetation period. We tested whether plant species richness affects consumer diversity directly (i), or indirectly through increased productivity (ii). Further, we tested the impact of plant community composition on arthropod diversity by testing for the effects of plant functional groups (iii). Abundance and species richness of both herbivores and carnivores increased with increasing plant species richness, but the underlying mechanisms differed between the two trophic groups. While higher species richness in herbivores was caused by an increase in resource diversity, carnivore richness was driven by plant productivity. Evenness of herbivore communities did not change along the gradient in plant species richness, whereas evenness of carnivores declined. The abundance of dominant herbivore species showed no response to changes in plant species richness, but the dominant carnivores were more abundant in species-rich plant communities. The functional composition of plant communities had small impacts on herbivore communities, whereas carnivore communities were affected by forbs of small stature, grasses and legumes. Contrasting patterns in the abundance of dominant species imply different levels of resource specialization for dominant herbivores (narrow food spectrum) and carnivores (broad food spectrum). That in turn could heavily affect ecosystem functions mediated by herbivorous and carnivorous arthropods, such as herbivory or biological pest control.

Positive interactions are ubiquitous processes within ecological communities that influence patterns of species diversity and ecosystem functioning. By reducing abiotic stress, such as desiccation, nurse plants positively affect (facilitate) associated plant species. Although plant‐plant interactions are well documented, consequences of plants on higher trophic levels are rarely examined. Here, we test for trophic consequences of the plant community by comparing visitation and diversity of pollinator and arthropod communities between cushion plants and non‐cushion plants throughout the season. Cushion plants were found to have significantly higher visitation rate and diversity of both arthropods and pollinators relative to all other non‐cushion plants. The positive effect of cushion plants found here can be explained for arthropods by cooler and more humid conditions and for pollinators by providing more abundant floral resources throughout the season. Although cushion plants have commonly been reported to facilitate other plants, this study shows that the cushion plant Silene acaulis has a positive effect on plants, arthropods, and pollinators with the greatest positive effect on pollinators. Other cushion plant species are likely also foundation species for many alpine trophic levels and have the capacity to stabilize species diversity at a community level by providing refuges for arthropods and resources for pollinators.

Research on the functional importance of biodiversity, motivated by global species loss, has documented that plant species richness affects many plant‐related ecosystem functions. Less is known about the effects of plant species richness on functions related to higher trophic levels, such as the consumption of biomass by animals, that is, herbivory. Previous studies have shown positive, neutral, or negative effects of plant species richness on herbivory. In the framework of a grassland biodiversity experiment (the Jena Experiment), we investigated herbivory (the proportion of leaf area damaged and the amount of leaf biomass consumed by arthropod herbivores) along two experimental gradients of plant species richness ranging from 1 to 60 species (Main Experiment) and from 1 to 8 species (Trait‐Based Experiment) biannually for five and three years, respectively. Additionally, plant functional diversity, based on traits related to plant growth, was manipulated as the number of functional groups in a community (Main Experiment) or a gradient of functional trait dissimilarity (Trait‐Based Experiment). Herbivory at the level of plant communities ranged from 0% to 31% (0 and 33.8 g/m2) in the Main Experiment and 0% to 8% (0 and 13.7 g/m2) in the Trait‐Based Experiment, and it was on average higher in summer than in spring. For both experimental gradients and all years investigated, we found a consistent increase in damaged leaf area and consumed biomass with increasing plant species richness. As mechanistic explanations for effects of plant species richness, we propose changes in plant quality and herbivore communities. The presence of specific plant functional groups significantly affected herbivory, likely related to traits affecting plant defense and nutritional value, but we found little evidence for effects of plant functional diversity. The general positive relationship between plant species richness and herbivory might contribute to effects of plant species richness on other ecosystem functions such as productivity and nutrient mineralization and can cascade up the food web also affecting higher trophic levels.

Experimental evidence shows that grassland plant diversity enhances ecosystem functioning. Yet, the transfer of results from controlled biodiversity experiments to naturally assembled ‘real world’ ecosystems remains challenging due to environmental variation among sites, confounding biodiversity ecosystem functioning relations in observational studies. To bridge the gap between classical biodiversity‐ecosystem functioning experiments and observational studies of naturally assembled and managed ecosystems, we created regionally replicated, within‐site gradients of species richness by seeding across agricultural grasslands differing in land‐use intensity (LUI) and abiotic site conditions. Within each of 73 grassland sites, we established a full‐factorial experiment with high‐diversity seeding and topsoil disturbance and measured 12 ecosystem functions related to productivity, and carbon and nutrient cycling after 4 years. We then analysed the effects of plant diversity (seeded richness as well as realized richness), functional community composition, land use and abiotic conditions on the ecosystem functions within (local scale) as well as among grassland sites (landscape scale). Despite the successful creation of a within‐site gradient in plant diversity (average increase in species richness in seeding treatments by 10%–35%), we found that only one to two of the 12 ecosystem functions responded to realized species richness, resulting in more closed nitrogen cycles in more diverse plant communities. Similar results were found when analysing the effect of the seeding treatment instead of realized species richness. Among sites, ecosystem functioning was mostly driven by environmental conditions and LUI. Also here, the only functions related to plant species richness were those associated with a more closed nitrogen cycle under increased diversity. The minor effects of species enrichment we found suggest that the functionally‐relevant niche space is largely saturated in naturally assembled grasslands, and that competitive, high‐functioning species are already present. Synthesis: While nature conservation and cultural ecosystem services can certainly benefit from plant species enrichment, our study indicates that restoration of plant diversity in naturally assembled communities may deliver only relatively weak increases in ecosystem functioning, such as a more closed nitrogen cycle, within the extensively to moderate intensively managed agricultural grasslands of our study.

Community structure and interaction webs of flower-visiting and cavity-nesting insects along an experimental plant diversity gradient