Biodiversity mediates the effects of stressors but not nutrients on litter decomposition
Léa Beaumelle Frederik De Laender Nico Eisenhauer
The consequences of real-world biodiversity change for ecosystem functioning depend on the type of global change driver and can be particularly significant when human activities decrease biodiversity.
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eLife
Human activities cause global environmental changes with important consequences for biodiversity and the functioning of ecosystems. Understanding these consequences is crucial for better policy and conservation strategies, which will ultimately promote human well-being too (IPBES, 2019). A key question is to what extent changes in ecosystem functioning are mediated by changes at which dimensions of biodiversity. Extensive research has demonstrated that biodiversity is needed for the stable provenance and enhancement of ecosystem processes and functions (Cardinale et al., 2012; Schuldt et al., 2018; Tilman et al., 2012). However, this body of evidence is mostly based on experiments comparing ecosystem functioning in artificial communities with varying number of species. Such experiments might not capture the complex ways by which shifts in biodiversity induced by global change ultimately affect ecosystem functioning (De Laender et al., 2016; Eisenhauer et al., 2019b).

Early biodiversity-ecosystem function (BEF) experiments typically controlled for environmental gradients, thus not accounting for the underlying drivers of biodiversity change (De Laender et al., 2016; Srivastava and Vellend, 2005; Wardle, 2016). These early experiments also focused on species richness as the sole biodiversity index, and manipulated it directly and randomly. However, environmental change will often elicit non-random changes in several facets of biodiversity (Eisenhauer et al., 2016; Giling et al., 2019; van der Plas, 2019) (community composition and population densities (Glassman et al., 2018; Spaak et al., 2017), functional diversity (Cadotte et al., 2011; Craven et al., 2018; Heemsbergen et al., 2004), trophic diversity (Soliveres et al., 2016; Wang and Brose, 2018; Zhao et al., 2019). The selective effects of environmental change emerge because organisms differ in their response to environmental change. For example, larger organisms and predators are often more negatively affected than smaller organisms at lower trophic levels (Hines et al., 2015; Sheridan and Bickford, 2011; Srivastava and Vellend, 2005; Voigt et al., 2007). Using realistic extinction scenarios, experiments found contrasting effects of non-random shifts in biodiversity on ecosystem functioning (e.g. Cárdenas et al., 2017; Jonsson et al., 2002; Melguizo-Ruiz et al., 2020; Oliveira et al., 2019; Smith and Knapp, 2003, Zavaleta and Hulvey, 2004). In addition, several variables that are not directly related to biodiversity control ecosystem functions (e.g. physiological rates [Dib et al., 2020; Thakur et al., 2018] and alterations of physical and chemical conditions [De Laender et al., 2016; Giling et al., 2019]). When environmental change affects these mechanisms, teasing out the relative importance of biodiversity-mediated effects is complicated even more. Given the number of different potential mechanisms, quantifying the extent to which shifts in biodiversity underpin the effect of environmental change on ecosystem functioning under real-world scenarios of global change is a key challenge for ecology (De Laender et al., 2016; Duffy et al., 2017; Eisenhauer et al., 2019b; Srivastava and Vellend, 2005; van der Plas, 2019; Wardle, 2016). Incorporating the impacts of environmental change drivers into BEF studies and meta-analyses is an important step forward to address such questions (De Laender et al., 2016; Eisenhauer et al., 2019b).

The vast majority of BEF experiments has focused on plant richness and ecosystem functions such as biomass production (van der Plas, 2019). However, litter decomposition has a tremendous importance in ecosystems and biogeochemical cycles (Follstad Shah et al., 2017). Small changes in the rate of this process can have important consequences for the overall carbon balance. Indeed, increases in decomposition rates could have positive feedback effects on climate warming by enhancing C losses (Kirschbaum, 2000). The diversity of decomposers (invertebrates and microorganisms that fragment and decompose organic matter in both aquatic and terrestrial systems) is crucial for litter decomposition (Eisenhauer et al., 2012; García-Palacios et al., 2013; Gessner et al., 2010; Handa et al., 2014; Hättenschwiler et al., 2005) and for other ecosystem functions as well (Eisenhauer et al., 2019a; Lefcheck et al., 2015; Schuldt et al., 2018). Despite the importance of decomposers, BEF experiments focusing on litter decomposition more often addressed the influence of plant litter diversity than of decomposers (Gessner et al., 2010; Tonin et al., 2018). In a meta-analysis, decomposer diversity had a greater effect on decomposition than the diversity of plant litter (Srivastava et al., 2009), although also weak and neutral effects have been reported (van der Plas, 2019). Facilitation and complementarity through niche partitioning are primary mechanisms underlying the positive relationship between decomposer diversity and decomposition (Gessner et al., 2010; Hättenschwiler et al., 2005; Tonin et al., 2018). Experiments conducted in natural conditions and reflecting realistic extinction scenarios are still relatively scarce, and demonstrate contrasting effects of non-random shifts in decomposer diversity on decomposition (Cárdenas et al., 2017; Jonsson et al., 2002; Melguizo-Ruiz et al., 2020; Wenisch et al., 2017). The need to quantify environmental change effects on decomposer diversity, along with potential knock-on effects on litter decomposition, is therefore particularly pressing.

There is a variety of environmental change drivers, and different types of drivers may have diverse effects on biodiversity and ecosystem functions (De Laender et al., 2016; Dib et al., 2020). We postulate that there are two main categories of environmental change: stressors and resource shifts. While stressors cannot be consumed, and act as conditions that alter growth rates (e.g., temperature, drought, chemical stressors), resources are by definition consumed (e.g., CO2 or mineral nutrients), which has important implications for how they should enter theory (Chase and Leibold, 2003; De Laender, 2018). Chemical stressors and nutrient enrichment are important case studies of environmental stressors and resource enrichment, because their presence is increasing rapidly (Bernhardt et al., 2017) and they are projected to have severe effects on biodiversity (Mazor et al., 2018). They are also of particular relevance for decomposer communities. Chemical stressors such as metals and pesticides decrease the diversity, abundance, growth and activity of decomposers across terrestrial and aquatic systems (e.g. Hogsden and Harding, 2012; Pelosi et al., 2014; Schäfer, 2019). In contrast, nutrient enrichment can have positive impacts on the abundance and physiological rates of decomposer organisms by reducing resource limitations (Treseder, 2008), but at the same time decrease decomposer diversity (Lecerf and Chauvet, 2008; Woodward et al., 2012). Across ecosystems, stressors and nutrients can exert opposite impacts on litter decomposition rates, with decreases in response to chemical stressors but increases following nutrient enrichment (Ferreira et al., 2015; Ferreira et al., 2016). In addition, decomposition involves both microorganisms and invertebrates (Bardgett and van der Putten, 2014; Gessner et al., 2010; Hättenschwiler et al., 2005) that may respond differently to stressors and nutrients with a higher sensitivity of invertebrates than microorganisms (Peters et al., 2013; Siebert et al., 2019). Although many published case studies report shifts in decomposer diversity and in rates of litter decomposition at sites impacted by stressors and nutrients, biodiversity-mediated effects have not yet been quantified across systems.

Here we addressed the question if the effects of stressors and nutrient enrichment on decomposer diversity and abundance explain the response of litter decomposition to these two types of pervasive environmental change drivers (Figure 1). We synthesized 69 published case studies reporting the impact of stressors (metals, pesticides) and nutrients (nitrogen or phosphorous additions) on litter decomposition and on decomposer diversity (taxa richness, Shannon diversity, evenness) or abundance (density, biomass) at sites differing in stressor or nutrient levels. Our comprehensive global dataset of 660 observations encompasses studies across taxonomic groups (animal (soil micro-, meso- and macrofauna, stream macroinvertebrates) and microbial (fungi and bacteria) decomposers), ecosystems (aquatic and terrestrial), and study types (experimental and observational) (Figure 2). We quantified the effect size of environmental change on decomposer diversity or abundance and on litter decomposition within studies using correlation coefficients between stressor or nutrient levels and decomposer diversity, abundance, and litter decomposition. We also characterized stressor and nutrient intensities, and standardized their levels in water, soil, or sediment using environmental quality criteria issued by environmental authorities (e.g. ECHA, USEPA, UKTAG). Using meta-analysis and structural equation modelling (SEM), we first compared the overall effects of stressors and nutrients on decomposers and decomposition across systems and studies (first meta-analysis), and second, addressed to what extent changes in decomposer diversity and abundance mediate the impacts of these two contrasting drivers of environmental change on decomposition (second meta-analysis and SEM). Third, we explored the effects of three main moderators on decomposers diversity, abundance, and decomposition responses, as found in the second meta-analysis: stressor or nutrient intensity, taxonomic group (animal vs. microbes) and study type (experimental vs. observational studies).