Biodiversity–ecosystem function experiments reveal the mechanisms underlying the consequences of biodiversity change in real world ecosystems

In a recent Forum paper, Wardle (Journal of Vegetation Science, 2016) questions the value of biodiversity–ecosystem function (BEF) experiments with respect to their implications for biodiversity changes in real world communities. The main criticism is that the previous focus of BEF experiments on random species assemblages within each level of diversity has ‘limited the understanding of how natural communities respond to biodiversity loss.’ He concludes that a broader spectrum of approaches considering both non‐random gains and losses of diversity is essential to advance this field of research. Wardle's paper is timely because of recent observations of frequent local and regional biodiversity changes across ecosystems. While we appreciate that new and complementary experimental approaches are required for advancing the field, we question criticisms regarding the validity of BEF experiments. Therefore, we respond by briefly reiterating previous arguments emphasizing the reasoning behind random species composition in BEF experiments. We describe how BEF experiments have identified important mechanisms that play a role in real world ecosystems, advancing our understanding of ecosystem responses to species gains and losses. We discuss recent examples where theory derived from BEF experiments enriched our understanding of the consequences of biodiversity changes in real world ecosystems and where comprehensive analyses and integrative modelling approaches confirmed patterns found in BEF experiments. Finally, we provide some promising directions in BEF research.     

Functional structure of biological communities predicts ecosystem multifunctionality

The accelerating rate of change in biodiversity patterns, mediated by ever increasing human pressures and global warming, demands a better understanding of the relationship between the structure of biological communities and ecosystem functioning (BEF). Recent investigations suggest that the functional structure of communities, i.e. the composition and diversity of functional traits, is the main driver of ecological processes. However, the predictive power of BEF research is still low, the integration of all components of functional community structure as predictors is still lacking, and the multifunctionality of ecosystems (i.e. rates of multiple processes) must be considered. Here, using a multiple-processes framework from grassland biodiversity experiments, we show that functional identity of species and functional divergence among species, rather than species diversity per se, together promote the level of ecosystem multifunctionality with a predictive power of 80%. Our results suggest that primary productivity and decomposition rates, two key ecosystem processes upon which the global carbon cycle depends, are primarily sustained by specialist species, i.e. those that hold specialized combinations of traits and perform particular functions. Contrary to studies focusing on single ecosystem functions and considering species richness as the sole measure of biodiversity, we found a linear and non-saturating effect of the functional structure of communities on ecosystem multifunctionality. Thus, sustaining multiple ecological processes would require focusing on trait dominance and on the degree of community specialization, even in species-rich assemblages.     

Species richness and trophic diversity increase decomposition in a co-evolved food web

Ecological communities show great variation in species richness, composition and food web structure across similar and diverse ecosystems. Knowledge of how this biodiversity relates to ecosystem functioning is important for understanding the maintenance of diversity and the potential effects of species losses and gains on ecosystems. While research often focuses on how variation in species richness influences ecosystem processes, assessing species richness in a food web context can provide further insight into the relationship between diversity and ecosystem functioning and elucidate potential mechanisms underpinning this relationship. Here, we assessed how species richness and trophic diversity affect decomposition rates in a complete aquatic food web: the five trophic level web that occurs within water-filled leaves of the northern pitcher plant, Sarracenia purpurea. We identified a trophic cascade in which top-predators--larvae of the pitcher-plant mosquito--indirectly increased bacterial decomposition by preying on bactivorous protozoa. Our data also revealed a facultative relationship in which larvae of the pitcher-plant midge increased bacterial decomposition by shredding detritus. These important interactions occur only in food webs with high trophic diversity, which in turn only occur in food webs with high species richness. We show that species richness and trophic diversity underlie strong linkages between food web structure and dynamics that influence ecosystem functioning. The importance of trophic diversity and species interactions in determining how biodiversity relates to ecosystem functioning suggests that simply focusing on species richness does not give a complete picture as to how ecosystems may change with the loss or gain of species.     

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.     

A general biodiversity–function relationship is mediated by trophic level

Species diversity affects the functioning of ecosystems, including the efficiency by which communities capture limited resources, produce biomass, recycle and retain biologically essential nutrients. These ecological functions ultimately support the ecosystem services upon which humanity depends. Despite hundreds of experimental tests of the effect of biodiversity on ecosystem function (BEF), it remains unclear whether diversity effects are sufficiently general that we can use a single relationship to quantitatively predict how changes in species richness alter an ecosystem function across trophic levels, ecosystems and ecological conditions. Our objective here is to determine whether a general relationship exists between biodiversity and standing biomass. We used hierarchical mixed effects models, based on a power function between species richness and biomass production (Y = a × S^b), and a database of 374 published experiments to estimate the BEF relationship (the change in biomass with the addition of species), and its associated uncertainty, in the context of environmental factors. We found that the mean relationship (b = 0.26, 95% CI: 0.16, 0.37) characterized the vast majority of observations, was robust to differences in experimental design, and was independent of the range of species richness levels considered. However, the richness–biomass relationship varied by trophic level and among ecosystems; in aquatic systems b was nearly twice as large for consumers (herbivores and detritivores) compared to primary producers; in terrestrial ecosystems, b for detritivores was negative but depended on few studies. We estimated changes in biomass expected for a range of changes in species richness, highlighting that species loss has greater implications than species gains, skewing a distribution of biomass change relative to observed species richness change. When biomass provides a good proxy for processes that underpin ecosystem services, this relationship could be used as a step in modeling the production of ecosystem services and their dependence on biodiversity.     

Community Biomass and Bottom up Multivariate Nutrient Complementarity Mediate the Effects of Bioturbator Diversity on Pelagic Production

Tests of the biodiversity and ecosystem functioning (BEF) relationship have focused little attention on the importance of interactions between species diversity and other attributes of ecological communities such as community biomass. Moreover, BEF research has been mainly derived from studies measuring a single ecosystem process that often represents resource consumption within a given habitat. Focus on single processes has prevented us from exploring the characteristics of ecosystem processes that can be critical in helping us to identify how novel pathways throughout BEF mechanisms may operate. Here, we investigated whether and how the effects of biodiversity mediated by non-trophic interactions among benthic bioturbator species vary according to community biomass and ecosystem processes. We hypothesized that (1) bioturbator biomass and species richness interact to affect the rates of benthic nutrient regeneration [dissolved inorganic nitrogen (DIN) and total dissolved phosphorus (TDP)] and consequently bacterioplankton production (BP) and that (2) the complementarity effects of diversity will be stronger on BP than on nutrient regeneration because the former represents a more integrative process that can be mediated by multivariate nutrient complementarity. We show that the effects of bioturbator diversity on nutrient regeneration increased BP via multivariate nutrient complementarity. Consistent with our prediction, the complementarity effects were significantly stronger on BP than on DIN and TDP. The effects of the biomass-species richness interaction on complementarity varied among the individual processes, but the aggregated measures of complementarity over all ecosystem processes were significantly higher at the highest community biomass level. Our results suggest that the complementarity effects of biodiversity can be stronger on more integrative ecosystem processes, which integrate subsidiary “simpler” processes, via multivariate complementarity. In addition, reductions in community biomass may decrease the strength of interspecific interactions so that the enhanced effects of biodiversity on ecosystem processes can disappear well before species become extinct.     

生物多样性与生态系统生产力：为什么野外观测和受控实验结果不一致？

 人们担心生物多样性的空前丧失会危及到生态系统的服务功能,因此有关生物多样性-生态系统生产力这一古老命题的讨论成为当今生态学的热点议题之一。20世纪90年代以David Tilman和Shahid Naeem为代表的生态学家利用大规模的受控实验,对物种多样性与生态系统功能的诸多方面进行     

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.     

Trophic complementarity drives the biodiversity–ecosystem functioning relationship in food webs

The biodiversity–ecosystem functioning (BEF) relationship is central in community ecology. Its drivers in competitive systems (sampling effect and functional complementarity) are intuitive and elegant, but we lack an integrative understanding of these drivers in complex ecosystems. Because networks encompass two key components of the BEF relationship (species richness and biomass flow), they provide a key to identify these drivers, assuming that we have a meaningful measure of functional complementarity. In a network, diversity can be defined by species richness, the number of trophic levels, but perhaps more importantly, the diversity of interactions. In this paper, we define the concept of trophic complementarity (TC), which emerges through exploitative and apparent competition processes, and study its contribution to ecosystem functioning. Using a model of trophic community dynamics, we show that TC predicts various measures of ecosystem functioning, and generate a range of testable predictions. We find that, in addition to the number of species, the structure of their interactions needs to be accounted for to predict ecosystem productivity.     

Plant community composition, not diversity, regulates soil respiration in grasslands

Soil respiration is responsible for recycling considerable quantities of carbon from terrestrial ecosystems to the atmosphere. There is a growing body of evidence that suggests that the richness of plants in a community can have significant impacts on ecosystem functioning, but the specific influences of plant species richness (SR), plant functional-type richness and plant community composition on soil respiration rates are unknown. Here we use 10-year-old model plant communities, comprising mature plants transplanted into natural non-sterile soil, to determine how the diversity and composition of plant communities influence soil respiration rates. Our analysis revealed that soil respiration was driven by plant community composition and that there was no significant effect of biodiversity at the three levels tested (SR, functional group and species per functional group). Above-ground plant biomass and root density were included in the analysis as covariates and found to have no effect on soil respiration. This finding is important, because it suggests that loss of particular species will have the greatest impact on soil respiration, rather than changes in biodiversity per se.     

A trait-based experimental approach to understand the mechanisms underlying biodiversity–ecosystem functioning relationships

Plant functional characteristics may drive plant species richness effects on ecosystem processes. Consequently, the focus of biodiversity–ecosystem functioning (BEF) experiments has expanded from the manipulation of plant species richness to manipulating functional trait composition. Involving ecophysiological plant traits in the experimental design might allow for a better understanding of how species loss alters ecosystem processes. Here we provide the theoretical background, design and first results of the ‘Trait-Based Biodiversity Experiment’ (TBE), established in 2010 that directly manipulates the trait composition of experimental plant communities.Analysis of six plant traits related to resource acquisition and use were analyzed using principal component analysis of 60 grassland species. The resulting two main axes describe gradients in functional similarity, and were used as the basis for designing plant communities with different functional and species diversity levels. Using such an approach allowed us to manipulate different levels of complementarity in spatial and temporal plant resource acquisition. In contrast to previous biodiversity experiments, the TBE is designed according to more realistic scenarios of non-random species loss along orthogonal axes of species trait dissimilarities. This allows us to tease apart the relative importance of selection and complementarity effects on multiple ecosystem processes, and to mechanistically study the consequences of plant community simplification.     

Heterogeneous microcommunities and ecosystem multifunctionality in seminatural grasslands under three management modes

Increasing attention has been paid to the relationship between biodiversity and ecosystem functioning (BEF) because of the rapid increase in species loss. However, over the past 20 years, most BEF studies only focused on the effect of species diversity on one or a few ecosystem functions, and only a few studies focused on ecosystem multifunctionality (i.e., the simultaneous provision of several ecosystem functions). Grassland ecosystems have important economic, environmental, and esthetic value; thus, this study focused on the heterogeneous microcommunities in grasslands under three management modes. The multifunctionality index (M‐index) was assessed at community and microcommunity scales, and the relationship between species diversity and multifunctionality was investigated. The communities were found to be respectively composed of one, three, and six microcommunities in grazing, clipping, and enclosure management, based on a two‐way indicator species analysis (TWINSPAN) and detrended correspondence analysis (DCA) for community structure. Biodiversity and soil indicators showed an apparent degradation of the grazing community, which had the worst M‐index. Clipping and enclosure communities showed no significant difference in biodiversity indices, soil variables, and M‐index; however, these indices were clearly different among microcommunities. Therefore, the microcommunity scale may be suitable to investigate the relationship between vegetation and multifunctionality in seminatural grassland ecosystems. Dominant species richness had more explanatory power for ecosystem multifunctionality than subdominant species richness, rare species richness, and the number of all species. Therefore, it is important to distinguish the role and rank of different species in the species richness–multifunctionality model; otherwise, the model might include redundant and unclear information. Communities with more codominant species whose distribution is also even might have better multifunctionality.     

Biodiversity change and ecosystem function in tropical forests

Recent debate about the fate of tropical forests has focused attention on the consequences of forest degradation and fragmentation for their diversity and composition, and the likely functional consequences of these changes. Existing data suggest that the responses of tropical forest plant and animal communities to habitat change are idiosyncratic, although a few consistent patterns are emerging. In particular, it is apparent that conventional diversity and richness metrics may not adequately represent anthropogenic changes to community structure and organisation. A widespread trend is towards ‘biotic homogenisation’: while disturbed forests may often have an equal or even a greater number of species than undisturbed forests, these species are typically drawn from a restricted pool; and endemic, restricted-range or habitat-specialist species are most likely to decline or go extinct. Similarly, studies have documented marked changes in the structure of food webs, even where the richness and diversity of component species remains little altered. What are the likely consequences of such changes for the important ecosystem functions performed by biodiversity, such as pollination and decomposition? Much of the extensive literature on the relationship between biodiversity and ecosystem function is of limited utility for answering this question, because experimental designs do not consider species-specific contributions to ecosystem function, abundance, degree of redundancy, or extinction-proneness; and few such studies have been carried out under realistic levels of diversity under field conditions, particularly in high-diversity ecosystems such as tropical forests. Furthermore, the focus has almost always been on richness as the explanatory variable, rather than the composition or structural attributes of communities. I briefly review recent papers that have begun to tackle these important issues, and consider how future research might help us understand the functional consequences of realistic changes to species composition and food-web ‘biostructure’ in tropical forests.     

Do experiments exploring plant diversity–ecosystem functioning relationships inform how biodiversity loss impacts natural ecosystems?

An enormous recent research effort focused on how plant biodiversity (notably species richness) influences ecosystem functioning, usually through experiments in which diversity is varied through random draws of species from a species pool. Such experiments are increasingly used to predict how species losses influence ecosystem functioning in ‘real’ ecosystems. However, this assumes that comparisons of experimental communities with low vs high species richness are analogous to comparisons of natural communities from which species either have or have not been lost. I explore the validity of this assumption, and highlight difficulties in using such experiments to draw conclusions about the ecosystem consequences of biodiversity loss in natural systems. Notably, these experiments do not mimic what happens in real ecosystems either when local extinctions occur or when species losses are offset by gains of new species. Despite limitations, this single experimental approach for studying how biodiversity loss affects ecosystems has often been advocated and implemented at the expense of other approaches; this limits understanding of how natural ecosystems respond to biodiversity loss. I conclude that a broader spectrum of approaches, and more explicit consideration of how species losses and gains operate in concert to influence ecosystems, will help progress this field.     

On the importance of the negative selection effect for the relationship between biodiversity and ecosystem functioning

Much of our knowledge on biodiversity and ecosystem functioning comes from studies examining the effects of biodiversity on biomass production within a trophic group. A large number of these studies have found that increasing biodiversity tends to increase biomass production, leading many ecologists to believe that there exists a general positive relationship between biodiversity and ecosystem functioning. Here we argue that such a positive relationship may not be general, particularly for ecosystem functions other than biomass. Our argument centers on the potential importance of the negative selection effect, which operates where competitively dominant species do not contribute significantly to the function of interest. We suggest that negative selection effects may be potentially common for non-biomass functions, for which species competitive ability may often be a poor indictor of its functional impact. We conclude that diverse (positive, negative, and neutral) BEF relationships are possible for non-biomass functions and that for a particular function, the exact form of the BEF relationship may depend on how species functional impacts relate to their competitive abilities in the community.     

青藏高原高寒草地生物多样性与生态系统功能的关系

生物多样性和生态系统功能(BEF)之间的关系是目前陆地生态系统生态学研究的热点, 对于生态系统的高效利用与管理意义重大, 而且对于退化生态系统功能的恢复及生物多样性的保护有重要的指导作用。高寒草地是青藏高原生态系统的主体, 近年来, 在气候变化与人为干扰等因素的驱动下, 高寒草地生态系统功能严重衰退。为此, 本文在综述物种多样性和生态系统功能及其相互关系研究进展的基础上, 首先从地下生态学过程研究、全球变化对生态系统多功能性的影响等方面解析了目前关于草地生物多样性和生态系统功能研究中存在的问题。继而, 从不同草地类型、草地退化程度、放牧、模拟气候变化、刈割、施肥、封育和补播等干扰利用方式对高寒草地物种多样性与生态系统功能的影响进行了全面的评述。并指出了高寒草地BEF研究中存在的不足, 今后应基于物种功能多样性开展高寒草地BEF研究, 全面且综合地考虑非生物因子(养分资源、外界干扰、环境波动等)对生物多样性与生态系统功能之间关系的影响, 关注尺度效应和要素耦合在全球气候变化对高寒草地BEF研究中的作用。最后, 以高寒草地BEF研究进展和结论为支撑依据, 综合提出了高寒草地资源利用和生物多样性保护的措施与建议: 加强放牧管理, 保护生物多样性; 治理退化草地, 维持生物多样性功能; 加强创新保护理念, 增强生态系统功能。     

种间互作网络的结构、生态系统功能及稳定性机制研究

生态群落中不同物种间发生多样化的相互作用, 形成了复杂的种间互作网络。复杂生态网络的结构如何影响群落的生态系统功能及稳定性是群落生态学的核心问题之一。种间互作直接影响到物质和能量在生态系统不同组分之间的流动和循环以及群落构建过程, 使得网络结构与生态系统功能和群落稳定性密切相关。在群落及生态系统水平上开展种间互作网络研究将为群落的构建机制、生物多样性维持、生态系统稳定性、物种协同进化和性状分化等领域提供新的视野。当前生物多样性及生态系统功能受到全球变化的极大影响, 研究种间互作网络的拓扑结构、构建机制、稳定性和生态功能也可为生物多样性的保护和管理提供依据。该文从网络结构、构建机制、网络结构和稳定性关系、种间互作对生态系统功能的影响等4个方面综述当前种间网络研究进展, 并提出在今后的研究中利用机器学习和多层网络等来探究环境变化对种间互作网络结构和功能的影响, 并实现理论和实证研究的有效整合。     

Resilience and stability of a pelagic marine ecosystem

The accelerating loss of biodiversity and ecosystem services worldwide has accentuated a long-standing debate on the role of diversity in stabilizing ecological communities and has given rise to a field of research on biodiversity and ecosystem functioning (BEF). Although broad consensus has been reached regarding the positive BEF relationship, a number of important challenges remain unanswered. These primarily concern the underlying mechanisms by which diversity increases resilience and community stability, particularly the relative importance of statistical averaging and functional complementarity. Our understanding of these mechanisms relies heavily on theoretical and experimental studies, yet the degree to which theory adequately explains the dynamics and stability of natural ecosystems is largely unknown, especially in marine ecosystems. Using modelling and a unique 60-year dataset covering multiple trophic levels, we show that the pronounced multi-decadal variability of the Southern California Current System (SCCS) does not represent fundamental changes in ecosystem functioning, but a linear response to key environmental drivers channelled through bottom-up and physical control. Furthermore, we show strong temporal asynchrony between key species or functional groups within multiple trophic levels caused by opposite responses to these drivers. We argue that functional complementarity is the primary mechanism reducing community variability and promoting resilience and stability in the SCCS.     

高寒草甸不同草地类型功能群多样性及组成对植物群落生产力的影响

对不同类型草地功能群多样性和组成与植物群落生产力之间的关系进行了探讨。结果表明：(1)在矮嵩草(Kobresia humlis)草甸和金露梅(Potentilla froticosa)灌丛中,豆科植物的作用比较明显,而其他功能群植物的作用较弱。(2)在藏嵩草(Kobresia tibetica)沼泽化草甸和小嵩草(K．pygmaca)草甸中,虽然杂类草、C3植物和莎草科植物功能群的生产力占群落初级生产力的比例较大,但二者在统计上没有显著性差异,这表明群落生产力除受物种多样性的影响外,也受物种本身特征和环境资源的影响,更主要的是受到功能群内物种密度和均匀度的影响,即功能群组成比功能群多样性更能说明对生态系统过程的影响。(3)不同类型草地群落植物功能群盖度与群落初级生产力呈显著的线性相关。(4)不同类型草地群落生产力与功能群内物种数的变化均表现为单峰曲线关系,即功能群内物种数处于中间水平时,群落生产力最高。     

Functional richness outperforms taxonomic richness in predicting ecosystem functioning in natural phytoplankton communities

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