Biodiversity influences ecosystem functioning in aquatic angiosperm communities

Knowledge of the connection between aquatic plant diversity and ecosystem processes is still limited. To examine how plant species diversity affects primary productivity, plant nutrient use, functional diversity of secondary producers and population/community stability, we manipulated submerged angiosperm species diversity in a field experiment lasting 15 weeks. Plant richness increased the shoot density for three of four species. Polyculture biomass production was enhanced by increasing richness, with positive complementarity and selection effects causing positive biodiversity effects. Species richness enhanced the community stability for biomass production and shoot density. Sediment ammonium availability decreased with plant diversity, suggesting improved nutrient usage with increasing plant richness. Interestingly, positive multitrophic effects of plant species richness on structural and functional diversity of macrobenthic secondary producers were recorded. The results suggest that mixed seagrass meadows play an important role for ecosystem functioning and thus contribute to the provision of goods and services in coastal areas.     

Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments

Recent experiments, mainly in terrestrial environments, have provided evidence of the functional importance of biodiversity to ecosystem processes and properties. Compared to terrestrial systems, aquatic ecosystems are characterised by greater propagule and material exchange, often steeper physical and chemical gradients, more rapid biological processes and, in marine systems, higher metazoan phylogenetic diversity. These characteristics limit the potential to transfer conclusions derived from terrestrial experiments to aquatic ecosystems whilst at the same time provide opportunities for testing the general validity of hypotheses about effects of biodiversity on ecosystem functioning. Here, we focus on a number of unique features of aquatic experimental systems, propose an expansion to the scope of diversity facets to be considered when assessing the functional consequences of changes in biodiversity and outline a hierarchical classification scheme of ecosystem functions and their corresponding response variables. We then briefly highlight some recent controversial and newly emerging issues relating to biodiversity‐ecosystem functioning relationships. Based on lessons learnt from previous experimental and theoretical work, we finally present four novel experimental designs to address largely unresolved questions about biodiversity‐ecosystem functioning relationships. These include (1) investigating the effects of non‐random species loss through the manipulation of the order and magnitude of such loss using dilution experiments; (2) combining factorial manipulation of diversity in interconnected habitat patches to test the additivity of ecosystem functioning between habitats; (3) disentangling the impact of local processes from the effect of ecosystem openness via factorial manipulation of the rate of recruitment and biodiversity within patches and within an available propagule pool; and (4) addressing how non‐random species extinction following sequential exposure to different stressors may affect ecosystem functioning. Implementing these kinds of experimental designs in a variety of systems will, we believe, shift the focus of investigations from a species richness‐centred approach to a broader consideration of the multifarious aspects of biodiversity that may well be critical to understanding effects of biodiversity changes on overall ecosystem functioning and to identifying some of the potential underlying mechanisms involved.     

Biodiversity effects on ecosystem functioning respond unimodally to environmental stress

Understanding how biodiversity (B) affects ecosystem functioning (EF) is essential for assessing the consequences of ongoing biodiversity changes. An increasing number of studies, however, show that environmental conditions affect the shape of BEF relationships. Here, we first use a game‐theoretic community model to reveal that a unimodal response of the BEF slope can be expected along environmental stress gradients, but also how the ecological mechanisms underlying this response may vary depending on how stress affects species interactions. Next, we analysed a global dataset of 44 experiments that crossed biodiversity with environmental conditions. Confirming our main model prediction, the effect of biodiversity on ecosystem functioning tends to be greater at intermediate levels of environmental stress, but varies among studies corresponding to differences in stress‐effects on species interactions. Together, these results suggest that increases in stress from ongoing global environmental changes may amplify the consequences of biodiversity changes.     

Biodiversity effects on ecosystem functioning change along environmental stress gradients

Positive relationship between biodiversity and ecosystem functioning has been observed in many studies, but how this relationship is affected by environmental stress is largely unknown. To explore this influence, we measured the biomass of microalgae grown in microcosms along two stress gradients, heat and salinity, and compared our results with 13 published case studies that measured biodiversity–ecosystem functioning relationships under varying environmental conditions. We found that positive effects of biodiversity on ecosystem functioning decreased with increasing stress intensity in absolute terms. However, in relative terms, increasing stress had a stronger negative effect on low‐diversity communities. This shows that more diverse biotic communities are functionally less susceptible to environmental stress, emphasises the need to maintain high levels of biodiversity as an insurance against impacts of changing environmental conditions and sets the stage for exploring the mechanisms underlying biodiversity effects in stressed ecosystems.     

Biodiversity and ecosystem functioning in aquatic microbial systems: a new analysis of temporal variation and species richness-predictability relations

Studies of microbial communities from aquatic ecosystems provide important insights into relations between various aspects of ecosystem functioning and changes in biodiversity. Aquatic microbial systems provide a valuable counterpoint to studies of terrestrial systems, because patterns reflect consequences of interactions occurring over many generations of community development, and are unlikely to represent artifacts of the initial conditions established in experimental communities. In this paper we re-analyse our previously published data to separate the contributions of temporal and spatial variation to overall variation in ecosystem functioning. A new analysis based on re-sampling confirms a negative relationship between richness and the variability of one ecosystem process, carbon dioxide flux. The negative relationship reflects high variation among communities of low species richness, rather than high temporal variation within communities of low richness. We also review the various transformations and summary statistics proposed as alternate measures of variability in ecosystem functioning, to point out that different measures are often appropriate for different kinds of data. Finally, we conclude that arguments about the cosmopolitan distribution of microbes do not preclude the existence of important relations between microbial species richness and ecosystem functioning.     

Biodiversity and ecosystem functioning: recent theoretical advances

The relationship between biodiversity and ecosystem functioning has emerged as a major scientific issue today. As experiments progress, there is a growing need for adequate theories and models to provide robust interpretations and generalisations of experimental results, and to formulate new hypotheses. This paper provides an overview of recent theoretical advances that have been made on the two major questions in this area: (1) How does biodiversity affect the magnitude of ecosystem processes (short‐term effects of biodiversity)? (2) How does biodiversity contribute to the stability and maintenance of ecosystem processes in the face of perturbations (long‐term effects of biodiversity)?
Positive short‐term effects of species diversity on ecosystem processes, such as primary productivity and nutrient retention, have been explained by two major types of mechanisms: (1) functional niche complementarity (the complementarity effect), and (2) selection of extreme trait values (the selection effect). In both cases, biodiversity provides a range of phenotypic trait variation. In the complementarity effect, trait variation then forms the basis for a permanent association of species that enhances collective performance. In the selection effect, trait variation comes into play only as an initial condition, and a selective process then promotes dominance by species with extreme trait values. Major differences between within‐site effects of biodiversity and across‐site productivity–diversity patterns have also been clarified. The local effects of diversity on ecosystem processes are expected to be masked by the effects of varying environmental parameters in across‐site comparisons.
A major reappraisal of the paradigm that has dominated during the last decades seems necessary if we are to account for long‐term effects of biodiversity on ecosystem functioning. The classical deterministic, equilibrium approaches to stability do not explain the reduced temporal variability of aggregate ecosystem properties that has been observed in more diverse systems. On the other hand, stochastic, nonequilibrium approaches do show two types of biodiversity effects on ecosystem productivity in a fluctuating environment: (1) a buffering effect, i.e., a reduction in the temporal variance; and (2) a performance‐enhancing effect, i.e., an increase in the temporal mean. The basic mechanisms involved in these long‐term insurance effects are very similar to those that operate in short‐term biodiversity effects: temporal niche complementarity, and selection of extreme trait values. The ability of species diversity to provide an insurance against environmental fluctuations and a reservoir of variation allowing adaptation to changing conditions may be critical in a long‐term perspective.
These recent theoretical developments in the area of biodiversity and ecosystem functioning suggest that linking community and ecosystem ecology is a fruitful avenue, which paves the way for a new ecological synthesis.     

生物多样性与生态系统功能:进展与争论

生物多样性与生态系统功能的关系已成为当前人类社会面临的一个重大科学问题,生物多样性的空前丧失,促使人们开展了大量研究工作来描述物种多样性-生态系统功能关系,并试图揭示多样性与系统功能关系的内在机制,本文将多样性对生态系统功能作用机制的有关假说分为统计学与生物学两大类：前者是从统计学角度来解释观察到的多样性-系统功能模式,包括抽样效应,统计均衡效应等;而后者是基于多样性的生物学效应给出的,包括生态位互补,种间正相互作用,保险效应等,本文较为详细地介绍了该领域内有代表性的实验工作,包括“生态箱”实验,Cedar Creek草地多样性实验,微宇宙实验,欧洲草地实验,以及在这些实验结果解释上的激烈争论。     

生物多样性与生态系统功能:最新的进展与动向

生物多样性与生态系统功能的关系及其内在机制是当前生态学领域的重大科学问题。 2 0 0 2年以来人们不再过多地纠缠于“抽样 -互补之争” ,对这一世纪课题的认识又有了新的进展。 (1)人们开始运用已有的知识揭示更大时间和空间尺度上的物种多样性 -生态系统功能关系。多样性作用机制可能存在着动态变化———“抽样向互补转型” :群落建立初期 ,抽样效应是主要的多样性作用机制 ;随时间推移 ,生态位互补成为主要机制。理论研究则预测 :局域尺度上生态系统功能与物种多样性呈现单峰曲线关系 ,在区域尺度上为单调上升关系 ;(2 )非生物因素与多样性 -生产力的交互关系吸引了许多实验研究。人们发现 :物种多样性 -生产力关系可能会受到资源供给率和环境扰动的修正 ,环境因素可能是多样性 -生产力关系的幕后操纵者 ;(3)人们开始重视营养级相互作用对于多样性 -生态系统功能关系的影响 ,生态位互补和抽样假说开始被扩展运用到消费者营养级上 ;(4 )人们开始认真思考物种共存机制在多样性 -生态系统功能关系的形成中所扮演的角色。理论模型研究表明 ,不同的物种共存机制会导致不同的多样性 -生产力关系     

The ecosystem functioning dimension in conservation: insights from remote sensing

An important goal of conservation biology is the maintenance of ecosystem processes. Incorporating quantitative measurements of ecosystem functions into conservation practice is important given that it provides not only proxies for biodiversity patterns, but also new tools and criteria for management. In the satellite era, the translation of spectral information into ecosystem functional variables expands and complements the more traditional use of satellite imagery in conservation biology. Remote sensing scientists have generated accurate techniques to quantify ecosystem processes and properties of key importance for conservation planning such as primary production, ecosystem carbon gains, surface temperature, albedo, evapotranspiration, and precipitation use efficiency; however, these techniques are still unfamiliar to conservation biologists. In this article, we identify specific fields where a remotely-sensed characterization of ecosystem functioning may aid conservation science and practice. Such fields include the management and monitoring of species and populations of conservation concern; the assessment of ecosystem representativeness and singularity; the use of protected areas as reference sites to assess global change effects; the implementation of monitoring and warning systems to guide adaptive management; the direct evaluation of supporting ecosystem services; and the planning and monitoring of ecological restorations. The approaches presented here illustrate feasible ways to incorporate the ecosystem functioning dimension into conservation through the use of satellite-derived information.     

Biodiversity and ecosystem functioning in naturally assembled communities

Approximately 25 years ago, ecologists became increasingly interested in the question of whether ongoing biodiversity loss matters for the functioning of ecosystems. As such, a new ecological subfield on Biodiversity and Ecosystem Functioning (BEF) was born. This subfield was initially dominated by theoretical studies and by experiments in which biodiversity was manipulated, and responses of ecosystem functions such as biomass production, decomposition rates, carbon sequestration, trophic interactions and pollination were assessed. More recently, an increasing number of studies have investigated BEF relationships in non‐manipulated ecosystems, but reviews synthesizing our knowledge on the importance of real‐world biodiversity are still largely missing. I performed a systematic review in order to assess how biodiversity drives ecosystem functioning in both terrestrial and aquatic, naturally assembled communities, and on how important biodiversity is compared to other factors, including other aspects of community composition and abiotic conditions. The outcomes of 258 published studies, which reported 726 BEF relationships, revealed that in many cases, biodiversity promotes average biomass production and its temporal stability, and pollination success. For decomposition rates and ecosystem multifunctionality, positive effects of biodiversity outnumbered negative effects, but neutral relationships were even more common. Similarly, negative effects of prey biodiversity on pathogen and herbivore damage outnumbered positive effects, but were less common than neutral relationships. Finally, there was no evidence that biodiversity is related to soil carbon storage. Most BEF studies focused on the effects of taxonomic diversity, however, metrics of functional diversity were generally stronger predictors of ecosystem functioning. Furthermore, in most studies, abiotic factors and functional composition (e.g. the presence of a certain functional group) were stronger drivers of ecosystem functioning than biodiversity per se. While experiments suggest that positive biodiversity effects become stronger at larger spatial scales, in naturally assembled communities this idea is too poorly studied to draw general conclusions. In summary, a high biodiversity in naturally assembled communities positively drives various ecosystem functions. At the same time, the strength and direction of these effects vary highly among studies, and factors other than biodiversity can be even more important in driving ecosystem functioning. Thus, to promote those ecosystem functions that underpin human well‐being, conservation should not only promote biodiversity per se, but also the abiotic conditions favouring species with suitable trait combinations.     

Biodiversity loss, trophic skew and ecosystem functioning

Experiments testing biodiversity effects on ecosystem functioning have been criticized on the basis that their random‐assembly designs do not reflect deterministic species loss in nature. Because previous studies, and their critics, have focused primarily on plants, however, it is underappreciated that the most consistent such determinism involves biased extinction of large consumers, skewing trophic structure and substantially changing conclusions about ecosystem impacts that assume changing plant diversity alone. Both demography and anthropogenic threats render large vertebrate consumers more vulnerable to extinction, on average, than plants. Importantly, species loss appears biased toward strong interactors among animals but weak interactors among plants. Accordingly, available evidence suggests that loss of a few predator species often has impacts comparable in magnitude to those stemming from a large reduction in plant diversity. Thus, the dominant impacts of biodiversity change on ecosystem functioning appear to be trophically mediated, with important implications for conservation.     

Biodiversity and ecosystem functioning decoupled: invariant ecosystem functioning despite non‐random reductions in consumer diversity

Most research that demonstrates enhancement and stabilization of ecosystem functioning due to biodiversity is based on biodiversity manipulations within one trophic level and measuring changes in ecosystem functions provided by that same trophic level. However, it is less understood whether and how modifications of biodiversity at one trophic level propagate vertically to affect those functions supplied by connected trophic levels or by the whole ecosystem. Moreover, most experimental designs in biodiversity–ecosystem functioning research assume random species loss, which may be of little relevance to non‐randomly assembled communities. Here, we used data from a published ecotoxicological experiment in which an insecticide gradient was applied as an environmental filter to shape consumer biodiversity. We tested how non‐random consumer diversity loss affected gross primary production (an ecosystem function provided by producers) and respiration (an ecosystem function provided by the ecosystem as whole) in species‐rich multitrophic freshwater communities (total of 128 macroinvertebrate and 59 zooplankton species across treatments). The insecticide decreased and destabilized macroinvertebrate and, to a lesser extent, zooplankton diversity. However, these effects on biodiversity neither affected nor destabilized any of the two studied ecosystem functions. The main reason for this result was that species susceptible to environmental filtering were different from those most strongly contributing to ecosystem functioning. The insecticide negatively affected the most abundant species, whereas much less abundant species had the strongest effects on ecosystem functioning. The latter finding may be explained by differences in body size and feeding guild membership. Our results indicate that biodiversity modifications within one trophic level induced by non‐random species loss do not necessarily translate into changes in ecosystem functioning supported by other trophic levels or by the whole community in the case of limited overlap between sensitivity and functionality.     

Biodiversity and ecosystem functioning: the mystery of the deep sea

Experiments performed in various ecosystems have shown a near-universal, saturating relationship between biodiversity and ecosystem processes. Analyses of deep-sea ecosystems challenge this generalisation and suggest that positive species interactions might be more widespread than previously believed.     

Biodiversity and ecosystem functioning: It is time for dispersal experiments

The experimental study of the relationship between biodiversity and ecosystem function has mainly addressed the effect of species and number of functional groups. In theory, this approach has mainly focused on how extinction affects function, whereas dispersal limitation of ecosystem function has been rarely discussed. A handful of seed introduction experiments, as well as numerous observations of the effects of long‐distance dispersal of alien species, indicate that ecosystem function may be strongly determined by dispersal limitation at the local, regional and/or global scales. We suggest that it is time to replace biodiversity manipulation experiments, based on random draw of species, with those addressing realistic scenarios of either extinction or dispersal. Experiments disentangling the dispersal limitation of ecosystem function should have to take into account the probability of arrival. The latter is defined as the probability that a propagule of a particular species will arrive at a particular community. Arrival probability depends on the dispersal ability and the number of propagules of a species, the distance a species needs to travel, and the permeability of the matrix landscape. Current databases, in particular those in northwestern and central Europe now enable robust estimation of arrival probability in plant communities. We suggest a general hypothesis claiming that dispersal limitation according to arrival probability will have ecosystem‐level effects different from those arising due to random arrival. This hypothesis may be rendered more region‐, landscape‐ or ecosystem‐specific by estimating arrival probabilities for different background conditions.     

Biodiversity and ecosystem functioning in food webs: the vertical diversity hypothesis

One challenge in merging community and ecosystem ecology is to integrate the complexity of natural multitrophic communities into concepts of ecosystem functioning. Here, we combine food‐web and allometry theories to demonstrate that primary production, as measured by the total nutrient uptake of the multitrophic community, is determined by vertical diversity (i.e. food web's maximum trophic level) and structure (i.e. distributions of species and their abundances and metabolic rates across trophic levels). In natural ecosystems, the community size distribution determines all these vertical patterns and thus the total nutrient uptake. Our model suggests a vertical diversity hypothesis (VDH) for ecosystem functioning in complex food webs. It predicts that, under a given nutrient supply, the total nutrient uptake increases exponentially with the maximum trophic level in the food web and it increases with its maximum body size according to a power law. The VDH highlights the effect of top–down regulation on plant nutrient uptake, which complements traditional paradigms that emphasised the bottom–up effect of nutrient supply on vertical diversity. We conclude that the VDH contributes to a synthetic framework for understanding the relationship between vertical diversity and ecosystem functioning in food webs and predicting the impacts of global changes on multitrophic ecosystems.     

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

In the past two decades, a large number of studies have investigated the relationship between biodiversity and ecosystem functioning, most of which focussed on a limited set of ecosystem variables. The Jena Experiment was set up in 2002 to investigate the effects of plant diversity on element cycling and trophic interactions, using a multi-disciplinary approach. Here, we review the results of 15 years of research in the Jena Experiment, focussing on the effects of manipulating plant species richness and plant functional richness. With more than 85,000 measures taken from the plant diversity plots, the Jena Experiment has allowed answering fundamental questions important for functional biodiversity research.First, the question was how general the effect of plant species richness is, regarding the many different processes that take place in an ecosystem. About 45% of different types of ecosystem processes measured in the ‘main experiment’, where plant species richness ranged from 1 to 60 species, were significantly affected by plant species richness, providing strong support for the view that biodiversity is a significant driver of ecosystem functioning. Many measures were not saturating at the 60-species level, but increased linearly with the logarithm of species richness. There was, however, great variability in the strength of response among different processes. One striking pattern was that many processes, in particular belowground processes, took several years to respond to the manipulation of plant species richness, showing that biodiversity experiments have to be long-term, to distinguish trends from transitory patterns. In addition, the results from the Jena Experiment provide further evidence that diversity begets stability, for example stability against invasion of plant species, but unexpectedly some results also suggested the opposite, e.g. when plant communities experience severe perturbations or elevated resource availability. This highlights the need to revisit diversity–stability theory.Second, we explored whether individual plant species or individual plant functional groups, or biodiversity itself is more important for ecosystem functioning, in particular biomass production. We found strong effects of individual species and plant functional groups on biomass production, yet these effects mostly occurred in addition to, but not instead of, effects of plant species richness.Third, the Jena Experiment assessed the effect of diversity on multitrophic interactions. The diversity of most organisms responded positively to increases in plant species richness, and the effect was stronger for above- than for belowground organisms, and stronger for herbivores than for carnivores or detritivores. Thus, diversity begets diversity. In addition, the effect on organismic diversity was stronger than the effect on species abundances.Fourth, the Jena Experiment aimed to assess the effect of diversity on N, P and C cycling and the water balance of the plots, separating between element input into the ecosystem, element turnover, element stocks, and output from the ecosystem. While inputs were generally less affected by plant species richness, measures of element stocks, turnover and output were often positively affected by plant diversity, e.g. carbon storage strongly increased with increasing plant species richness. Variables of the N cycle responded less strongly to plant species richness than variables of the C cycle.Fifth, plant traits are often used to unravel mechanisms underlying the biodiversity–ecosystem functioning relationship. In the Jena Experiment, most investigated plant traits, both above- and belowground, were plastic and trait expression depended on plant diversity in a complex way, suggesting limitation to using database traits for linking plant traits to particular functions.Sixth, plant diversity effects on ecosystem processes are often caused by plant diversity effects on species interactions. Analyses in the Jena Experiment including structural equation modelling suggest complex interactions that changed with diversity, e.g. soil carbon storage and greenhouse gas emission were affected by changes in the composition and activity of the belowground microbial community. Manipulation experiments, in which particular organisms, e.g. belowground invertebrates, were excluded from plots in split-plot experiments, supported the important role of the biotic component for element and water fluxes.Seventh, the Jena Experiment aimed to put the results into the context of agricultural practices in managed grasslands. The effect of increasing plant species richness from 1 to 16 species on plant biomass was, in absolute terms, as strong as the effect of a more intensive grassland management, using fertiliser and increasing mowing frequency. Potential bioenergy production from high-diversity plots was similar to that of conventionally used energy crops. These results suggest that diverse ‘High Nature Value Grasslands’ are multifunctional and can deliver a range of ecosystem services including production-related services.A final task was to assess the importance of potential artefacts in biodiversity–ecosystem functioning relationships, caused by the weeding of the plant community to maintain plant species composition. While the effort (in hours) needed to weed a plot was often negatively related to plant species richness, species richness still affected the majority of ecosystem variables. Weeding also did not negatively affect monoculture performance; rather, monocultures deteriorated over time for a number of biological reasons, as shown in plant-soil feedback experiments.To summarize, the Jena Experiment has allowed for a comprehensive analysis of the functional role of biodiversity in an ecosystem. A main challenge for future biodiversity research is to increase our mechanistic understanding of why the magnitude of biodiversity effects differs among processes and contexts. It is likely that there will be no simple answer. For example, among the multitude of mechanisms suggested to underlie the positive plant species richness effect on biomass, some have received limited support in the Jena Experiment, such as vertical root niche partitioning. However, others could not be rejected in targeted analyses. Thus, from the current results in the Jena Experiment, it seems likely that the positive biodiversity effect results from several mechanisms acting simultaneously in more diverse communities, such as reduced pathogen attack, the presence of more plant growth promoting organisms, less seed limitation, and increased trait differences leading to complementarity in resource uptake. Distinguishing between different mechanisms requires careful testing of competing hypotheses. Biodiversity research has matured such that predictive approaches testing particular mechanisms are now possible.