Effects of biodiversity strengthen over time as ecosystem functioning declines at low and increases at high biodiversity

Human-caused declines in biodiversity have stimulated intensive research on the consequences of biodiversity loss for ecosystem services and policy initiatives to preserve the functioning of ecosystems. Short-term biodiversity experiments have documented positive effects of plant species richness on many ecosystem functions, and longer-term studies indicate, for some ecosystem functions, that biodiversity effects can become stronger over time. Theoretically, a biodiversity effect can strengthen over time by an increasing performance of high-diversity communities, by a decreasing performance of low-diversity communities, or a combination of both processes. Which of these two mechanisms prevail, and whether the increase in the biodiversity effect over time is a general property of many functions remains currently unclear. These questions are an important knowledge gap as a continuing decline in the performance of low-diversity communities would indicate an ecosystem-service debt resulting from delayed effects of species loss on ecosystem functioning. Conversely, an increased performance of high-diversity communities over time would indicate that the benefits of biodiversity are generally underestimated in short-term studies. Analyzing 50 ecosystem variables over 11 years in the world's largest grassland biodiversity experiment, we show that overall plant diversity effects strengthened over time. Strengthening biodiversity effects were independent of the considered compartment (above- or belowground), organizational level (ecosystem variables associated with the abiotic habitat, primary producers, or higher trophic levels such as herbivores and pollinators), and variable type (measurements of pools or rates). We found evidence that biodiversity effects strengthened because of both a progressive decrease in functioning in species-poor and a progressive increase in functioning in species-rich communities. Our findings provide evidence that negative feedback effects at low biodiversity are as important for biodiversity effects as complementarity among species at high biodiversity. Finally, our results indicate that a current loss of species will result in a future impairment of ecosystem functioning, potentially decades beyond the moment of species extinction

δ¹⁸O and δ²H values of xylem water before and after the labeling.

<p>δ¹⁸O (top) and δ²H (bottom) values are given for the background samples and the samples taken after the labeling at three different times (April, June, September 2011) in each case pooled for all species richness levels. Outliers (at δ¹⁸O = 141.7 ‰ and δ²H = 101.3 ‰ in June and at δ¹⁸O = 187.3 ‰ in September) were removed for reasons of clarity. Results of the corresponding mixed-effects models are given in the running text. Significant differences among the background samples and the samples taken after labeling are indicated with asterisks (with *** referring to <i>P</i> < 0.001).</p

Summary of the mixed-effects model testing the effects of species richness, functional group number and functional group identity on xylem water enrichment in ¹⁸O and ²H (i.e., difference between samples taken after the labeling and the background samples).

<p>Analyses were carried out for each campaign separately.</p><p>Summary of the mixed-effects model testing the effects of species richness, functional group number and functional group identity on xylem water enrichment in ¹⁸O and ²H (i.e., difference between samples taken after the labeling and the background samples).</p

δ¹⁸O and δ²H values of soil water before and after the labeling.

<p>δ¹⁸O (A, C, E) and δ²H (B, D, F) values of soil water labeled with ¹⁸O-enriched water in upper soil depths and with ²H-enriched water in lower soil depths. Grey bands illustrate depths of tracer application. Data are given for the natural background soil as well as after the labeling at three different times in 2011 (April: A-B, June: C-D, September: E-F) in each case pooled for all species richness levels. Values of soil water content (SWC) in 8, 16 and 32 cm are given as mean ± 1 SD for the 4-day labeling and harvest campaigns.</p

Data from: Below-ground resource partitioning alone cannot explain the biodiversity–ecosystem function relationship: a field test using multiple tracers

1. Belowground resource partitioning is among the most prominent hypotheses for driving the positive biodiversity-ecosystem function relationship. However, experimental tests of this hypothesis in biodiversity experiments are scarce, and the available evidence is not consistent. 2. We tested the hypothesis that resource partitioning in space, in time, or in both space and time combined drives the positive effect of diversity on both plant productivity and community resource uptake. At the community level, we predicted that total community resource uptake and biomass production above- and belowground will increase with increased species richness or functional group richness. We predicted that at the species level resource partition breadth will become narrower, and that overlap between the resource partitions of different species will become smaller with increasing species richness or functional group richness. 3. We applied multiple resource tracers (Li and Rb as potassium analogues, the water isotopologues - H218O and 2H2O, and 15N) in three seasons at two depths across a species and functional group richness gradient at a grassland biodiversity experiment. We used this multidimensional resource tracer study to test if plant species partition resources with increasing plant diversity across space, time, or both simultaneously. 4. At the community level, community resource uptake of nitrogen and potassium and above- and belowground biomass increased significantly with increasing species richness but not with increasing functional group richness. However, we found no evidence that resource partition breadth or resource partition overlap decreased with increasing species richness for any resource in space, time, or both space and time combined. Synthesis: These findings indicate that belowground resource partitioning may not drive the enhanced resource uptake or biomass production found here. Instead, other mechanisms such as facilitation, species-specific biotic feedback, or aboveground resource partitioning are likely necessary for enhanced overall ecosystem function

Data from: Below-ground resource partitioning alone cannot explain the biodiversity–ecosystem function relationship: a field test using multiple tracers

1. Belowground resource partitioning is among the most prominent hypotheses for driving the positive biodiversity-ecosystem function relationship. However, experimental tests of this hypothesis in biodiversity experiments are scarce, and the available evidence is not consistent. 2. We tested the hypothesis that resource partitioning in space, in time, or in both space and time combined drives the positive effect of diversity on both plant productivity and community resource uptake. At the community level, we predicted that total community resource uptake and biomass production above- and belowground will increase with increased species richness or functional group richness. We predicted that at the species level resource partition breadth will become narrower, and that overlap between the resource partitions of different species will become smaller with increasing species richness or functional group richness. 3. We applied multiple resource tracers (Li and Rb as potassium analogues, the water isotopologues - H218O and 2H2O, and 15N) in three seasons at two depths across a species and functional group richness gradient at a grassland biodiversity experiment. We used this multidimensional resource tracer study to test if plant species partition resources with increasing plant diversity across space, time, or both simultaneously. 4. At the community level, community resource uptake of nitrogen and potassium and above- and belowground biomass increased significantly with increasing species richness but not with increasing functional group richness. However, we found no evidence that resource partition breadth or resource partition overlap decreased with increasing species richness for any resource in space, time, or both space and time combined. Synthesis: These findings indicate that belowground resource partitioning may not drive the enhanced resource uptake or biomass production found here. Instead, other mechanisms such as facilitation, species-specific biotic feedback, or aboveground resource partitioning are likely necessary for enhanced overall ecosystem function

Long-term study of root biomass in a biodiversity experiment reveals shifts in diversity effects over time

Biodiversity experiments generally report a positive effect of plant biodiversity on aboveground biomass (overyielding), which typically increases with time. Various studies also found overyielding for belowground plant biomass, but this has never been measured over time. Also, potential underlying mechanisms have remained unclear. Differentiation in rooting patterns among plant species and plant functional groups has been proposed as a main driver of the observed biodiversity effect on belowground biomass, leading to more efficient belowground resource use with increasing diversity, but so far there is little evidence to support this. We analyzed standing root biomass and its distribution over the soil profile, along a 1–16 species richness gradient over eight years in the Jena Experiment in Germany, and compared belowground to aboveground overyielding. In our long-term dataset, total root biomass increased with increasing species richness but this effect was only apparent after four years. The increasingly positive relationship between species richness and root biomass, explaining 12% of overall variation and up to 28% in the last year of our study, was mainly due to decreasing root biomass at low diversity over time. Functional group composition strongly affected total standing root biomass, explaining 44% of variation, with grasses and legumes having strong overall positive and negative effects, respectively. Functional group richness or interactions between functional group presences did not strongly contribute to overyielding. We found no support for the hypothesis that vertical root differentiation increases with species richness, with functional group richness or composition. Other explanations, such as stronger negative plant–soil feedbacks in low-diverse plant communities on standing root biomass and vertical distribution should be considered

Below-ground complementarity effects in a grassland biodiversity experiment are related to deep-rooting species

Below-ground resource partitioning is often proposed as the underlying mechanism for the positive relationship between plant species richness and productivity. For example, if species have different root distributions, a mixture of plant species may be able to use the available resources more completely than the individual species in a monoculture. However, there is little experimental evidence for differentiation in vertical root distributions among species and its contribution to biodiversity effects. We determined species-specific root standing biomass over depth using molecular techniques (real-time qPCR) in a large grassland biodiversity experiment (one to eight plant species mixtures), in 2 years. Species-specific root biomass data were used to disentangle the effects of positive interactions between species (complementarity effects) and effects due to dominance of productive species (selection effects) on root biomass in mixtures. In a next step, these biodiversity effects were linked to the diversity of rooting depths and the averaged rooting depth of the community. Root biomass increased with species richness. This was mainly due to positive interactions (the complementarity effect), which increased with species richness below-ground. In contrast, the selection effect decreased with species richness. Although there was considerable variation in vertical root distribution between species in monocultures, the diversity of rooting strategies did not explain the complementarity effect. Rather, the abundance of deep-rooting species in mixtures (i.e. high community-weighted mean) was significantly related to the complementarity effect. Comparing the "predicted" root distribution (based on monocultures) to the actual distribution in mixtures, we found that mixtures rooted deeper than expected, but this did not better explain the complementarity effect. Synthesis. This study demonstrates that vertical root distributions of species provide only subtle evidence for resource partitioning. We found no evidence that functional diversity in vertical rooting patterns was important for the complementarity effect, in contrast to our expectation that the enhancement of productivity was due to resource partitioning. Alternatively, we found significant but weak relationships between the complementarity effect and deep-rooting communities, based on the community-weighted mean root distribution. This suggests that factors other than below-ground resource partitioning alone may drive the biodiversity-productivity relationship.</p

Data from: Belowground complementarity effects in a grassland biodiversity experiment are related to deep-rooting species

1. Belowground resource partitioning is often proposed as the underlying mechanism for the positive relationship between plant species richness and productivity. For example, if species have different root distributions, a mixture of plant species may be able to use the available resources more completely than the individual species in a monoculture. However, there is little experimental evidence for differentiation in vertical root distributions among species and its contribution to biodiversity effects. 2. We determined species-specific root standing biomass over depth using molecular techniques (real time-qPCR) in a large grassland biodiversity experiment (1-8 plant species mixtures), in two years. Species-specific root biomass data were used to disentangle the effects of positive interactions between species (complementarity effects) and effects due to dominance of productive species (selection effects) on root biomass in mixtures. In a next step, these biodiversity effects were linked to the diversity of rooting depths and the averaged rooting depth of the community. 3. Root biomass increased with species richness. This was mainly due to positive interactions (the complementarity effect), which increased with species richness belowground. In contrast, the selection effect decreased with species richness. Although there was considerable variation in vertical root distribution between species in monocultures, the diversity of rooting strategies did not explain the complementarity effect. Rather, the abundance of deep-rooting species in mixtures (i.e. high community weighted mean) was significantly related to the complementarity effect. Comparing the ‘predicted’ root distribution (based on monocultures) to the actual distribution in mixtures, we found that mixtures rooted deeper than expected, but this did not better explain the complementarity effect. 4. Synthesis: This study demonstrates that vertical root distributions of species provide only subtle evidence for resource partitioning. We found no evidence that functional diversity in vertical rooting patterns was important for the complementarity effect, in contrast to our expectation that the enhancement of productivity was due to resource partitioning. Alternatively, we found significant but weak relationships between the complementarity effect and deep-rooting communities, based on the community weighted mean root distribution. This suggests that factors other than belowground resource partitioning alone may drive the biodiversity-productivity relationship