Biol. Rev. (2019), 94, pp. 1220–1245. 1220 doi: 10.1111/brv.12499 Biodiversity and ecosystem functioning in naturally assembled communities Fons van der Plas∗ Systematic Botany and Functional Biodiversity, Institute of Biology, Leipzig University, Johannisallee 21-23, 04103 Leipzig, Germany ABSTRACT 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. Key words: biodiversity, community composition, context dependence, ecosystem functioning, ecosystem multifunctionality, environment, global change, land use, spatial scale. CONTENTS I. Introduction ..............................................................................................1221 II. Quantitative response of ecosystem functioning to biodiversity in naturally assembled communities .....1222 (1) Literature search .....................................................................................1223 (2) Spread of evidence ...................................................................................1223 (3) Balance of evidence ..................................................................................1225 (a) Biomass ...........................................................................................1225 (b) Litter decomposition ..............................................................................1227 (c) Soil organic carbon storage .......................................................................1228 * Address for correspondence (Tel: +49-341-97-38587; E-mail: [email protected]) Biological Reviews 94 (2019) 1220–1245 © 2019 Cambridge Philosophical Society Biodiversity and ecosystem functioning in the wild 1221 (d) Biomass stability ..................................................................................1228 (e) Pathogen and herbivore damage .................................................................1229 (f ) Pollination ........................................................................................1230 (g) Ecosystem multifunctionality .....................................................................1230 (4) Effects of sampling design ............................................................................1230 III. Relative importance of biodiversity ......................................................................1231 (1) Effects of biodiversity versus those of functional composition and abiotic factors ......................1231 (2) Relative roles of taxonomic, functional and phylogenetic diversity ...................................1234 (3) The relative importance of biodiversity across spatial scales ..........................................1235 IV. Future directions .........................................................................................1236 V. Conclusions ..............................................................................................1236 VI. Acknowledgements .......................................................................................1236 VII. References ................................................................................................1237 VIII. Supporting Information ..................................................................................1245 I. INTRODUCTION 2011; Tilman, Isbell & Cowles, 2014; Isbell et al., 2017) and the focus of this review, is how important biodiversity is in The 1992 Earth Summit in Rio de Janeiro increased driving various ecosystem processes in non-manipulated, interest in the question of how changes in biodiversity, naturally assembled communities. In natural systems, and species loss in particular, affect the functioning of variation in biodiversity is non-randomly distributed across ecosystems (Schulze & Mooney, 1993). Soon after, some space and time, and driven by various environmental of the first publications experimentally linking biodiversity factors, as well as by ecosystem functions such as plant with ecosystem functioning emerged (Naeem et al., 1994; biomass (Grime, 1973; Hautier, Niklaus & Hector, 2009) Tilman, Wedin & Knops, 1996). These studies represented a (Fig. 1C). There are various reasons why BEF relationships in major paradigm shift in ecological thinking. Until that time, naturally assembled communities might deviate from those biodiversity was mainly thought of as factor that responds in experimental communities. First, in most experiments, to environmental change and ecosystem functions (Fig. 1A), biodiversity loss is random, and variation in abiotic conditions but not as something that also drives ecosystem functioning is minimized. The question is whether the mechanisms (Fig. 1C) (Naeem, 2002; Hillebrand & Matthiessen, 2009; that drive BEF relationships in such simplified systems Tilman, Isbell & Cowles, 2014). Thus, a new scientific are strong enough also to have a major impact in much sub-discipline on ‘Biodiversity and Ecosystem Functioning’ more complex, real-world systems, where other community (BEF) was born. aspects not related to biodiversity per se (e.g. the presence The BEF field was initially dominated by theoretical (e.g. of a keystone species) or abiotic conditions may outweigh Tilman, Lehman & Thomson, 1997; Loreau, 1998) and any biodiversity effects (Díaz & Cabido, 2001; Lavorel & experimental studies (e.g. Tilman, Wedin & Knops, 1996; Garnier, 2002; Díaz et al., 2007). Second, in most BEF Hector et al., 1999; Roscher et al., 2003), where researchers experiments, immigration of new species into communities typically simulated random biodiversity (e.g. species) loss is not allowed (and avoided by e.g. weeding). This contrasts [but see Naeem et al., 1994 and Tilman & Downing, 1994, with real-world situations, and both theoretical (e.g. Leibold, where biodiversity loss was non-random], and measured the Chase & Ernest, 2017) and empirical studies (Petermann responses of certain ecosystem functions, such as biomass et al., 2010; Veen, van der Putten & Bezemer, 2018) suggest production or litter decomposition. As such, BEF research that BEF relationships might be weaker in open communities, initially focused on the causal effects of biodiversity on in part because species-poor communities tend to get invaded ecosystem functioning, in simplified systems where variation by species that increase their biomass production. Third, in in other factors than biodiversity was minimal (Fig. 1B). The naturally assembled communities, there can be feedbacks aim of these studies was to investigate whether biodiversity from ecosystem functions to biodiversity (Grace et al., 2016). can drive ecosystem functioning, rather than to assess For example, in grasslands with high biomass production, the strength of these effects in the real world. Various various species can be forced to extinction due to competition papers synthesizing this work have emerged, and based for light (Grime, 1973; Hautier, Niklaus