Evaluation of hysteretic responses in the ecosystem
Finally, we evaluated if ecosystem thresholds were indicative of hysteretic responses to land use, by determining whether responses were different when LUI and its components increased or decreased over time. If hysteretic responses occur, we would expect different trajectories of diversity and function change when LUI increases or decreases, and therefore a higher threshold along the LUI gradient when land use is intensified. Therefore, for each plot we determined whether LUI had increased from the previous year (land use intensification) or decreased from the previous year (land use extensification). All cases where land use did not change between years were excluded. We also did not consider mowing as there were not enough thresholds to test for hysteresis. We analyzed all variables for which we had identified a threshold response to LUI and repeated the threshold detection analysis to test for different thresholds when land use had recently increased or decreased. If hysteresis occurs, then we would expect lower thresholds if land use has recently decreased (extensification). Specifically, for each combination of variable and year we ran a separate analysis for those plots that had experienced intensification or extensification. We ran individual analyses for each year because plots could show periods of increasing or decreasing land use at different times (on average across years; LUI: intensification = 71.9 ± 3.3 plots, extensification = 71.5 ± 3.2; Grazing: intensification = 55 ± 2.9 plots, extensification = 54 ± 3; Fertilization: intensification = 30.6 ± 1.5 plots, extensification = 33.6 ± 1.4;). Finally, we tested if the thresholds for plots undergoing intensification or extensification differed significantly, as an indicator of hysteretic dynamics. To do this, we fitted a linear mixed effect model using plot category (intensification and extensification) and variable type (diversity or function), together with their interaction, as explanatory fixed variables, threshold value as the response variable and year as a random factor. Linear mixed effect models were fitted with the lme4 package in R (Bates et al. 2015). All statistical analysis were done with R 3.6.2 (R Development Core Team 2014).
Results
Identification of ecological thresholds
We found that almost a third (29.3%) of the diversities and ecosystem functions responded non-linearly to land use intensification (Table S4.1). We found more non-linear responses for diversities (9 of the 21 taxa) than for functions (2 of the 16 functions). In general, aboveground taxa showed more non-linear responses to land use (5 of the 10 taxa), than belowground taxa (2 fungal guilds out of the 11 taxa). For the 11 variables which showed non-linear responses to land use intensification, we identified 9 (diversity of 7 taxa and 2 functions, Figure 2) with a threshold response. Thresholds were remarkably consistent between variables and were around a land use intensity (LUI) value of 1 (most aboveground diversity metrics) and 1.5-2 (fungal diversity, plant shoot biomass and N retention). To better understand what this threshold means we calculated the mean value of individual components across the 24 plots with average LUI within the expected threshold value (LUI = 1.42 ± 0.12): grazing = 130.9 ± 24.5 livestock units · grazing days · ha-1 · year-1; mowing = 1 ± 0.2 cuts · year-1; and fertilization = 4.9 ± 1.6 kg N · ha-1 · year-1. The transition threshold is therefore associated with a switch from lightly grazed, unfertilized grasslands, to fertilized, and frequently mown or grazed grasslands.
We also found that diversities of several trophic levels and functions had threshold responses to each land use component (Figure S1.1-3). Most of these thresholds occurred at very low levels, which probably represents a threshold between the presence or absence of any land use component (31% of grasslands considered were not grazed, 35% were not mown and 60% were unfertilized).
Early warning signals at ecological thresholds
We found most variables showed an increase in variance at LUI values close to, or within, the thresholds, although only a third of them showed a significant increase in variance, relative to random expectations (3 of 9, vascular plants, lichens and vertebrates granivores, Figure 3). However, we also observed significant increases in variance at a similar LUI values for some belowground variables that did not show a threshold response to land use intensity (e.g.Symbiotic fungi, Bacteria, Root biomass, Figure S2).
Hysteretic responses in the ecosystem
We found that thresholds for ecosystem functions occurred at higher LUI than for biodiversity (Figure 4). Additionally, these LUI thresholds observed for ecosystem functions occurred at lower land use levels in plots where LUI had decreased compared to the previous year (extensification) than in plots where LUI had increased (intensification, Figure 4, Figure S3). This indicates that the observed critical transition for functions in grasslands is hysteretic and returning to previous functioning levels requires lower land use intensity than is needed to change functioning as land use is intensified.
Discussion
Identification of ecological thresholds
Our analysis found that, in general, aboveground taxa were more likely to show threshold responses to land use intensity while belowground diversity and ecosystem functions had more linear responses. This agrees with findings showing that biodiversity is more likely to show a non-linear response to management (Evans et al. 2017), and often declines non-linearly with land use intensification (Kleijn et al. 2009; Allan et al. 2015). However, while land use intensification reduces aboveground diversity by homogenizing environmental conditions, by increasing arthropod mortality (grazing and mowing) or by favoring particular species (fertilization), belowground diversity may be increased by nutrients inputs to the soil (Chen & Wise 1999). In addition, the long management history of the studied grasslands may have reduced belowground responses to land use intensity, as many belowground communities may be affected more by soil history than recent changes in aboveground composition (Elgersma et al.2011). Regarding functions, the lack of non-linear responses could be explained by ecological redundancy (Walker 1992). It is possible that the loss of functionally important species with land use intensification can be partially compensated for by the remaining species, thus reducing abrupt responses (Muradian 2001). These contrasting responses of biodiversity (above and belowground) and ecosystem functioning highlight the need for system level approaches to understand overall consequences of land use intensification.
Remarkably, all variables showed thresholds at similar land use intensity (LUI) values. This might suggest that plant communities undergo a regime shift due to land use intensification that cascades to other taxa and functions. We observed two types of grasslands: extensively managed (LUI < 1) grasslands, with high aboveground diversity (especially of primary producers and vertebrates) and high nutrient retention, which are lightly grazed and unfertilized and intensively managed (LUI > 1.5) productive grasslands with high belowground fungal diversity (Figure 2), which are fertilized and mown or intensively grazed. Low grazing intensities promote plant diversity by limiting dominant species (Maurer et al. 2006; Bochet al. 2016; Busch et al. 2019), while the fertilizer addition associated with higher mowing frequencies selects for more competitive, taller and faster-growing plants at the expense of smaller and slower-growing ones (Gough et al. 2001; Dickson et al.2014; DeMalach et al. 2017; Busch et al. 2019). In the case of vertebrates, intensification in grasslands reduces diversity by limiting nesting options and increasing the risk of nest discovery by predators (Verhulst et al. 2004). In addition, biodiversity losses can cascade between trophic groups, as a reduction in primary-producer diversity affects herbivores by reducing the diversity of resources available to them (Uchida & Ushimaru 2014). Fertilization and increased dominance of fast-growing species in intensive grasslands affects ecosystem functioning by increasing aboveground plant biomass (Lavorel & Grigulis 2012; Allan et al. 2015). However, this increase may be non-linear, as environmental factors (e.g. soil water levels and light) limit further increases in biomass (Kleinebeckeret al. 2014), or because the diversity loss associated with high fertilizer inputs results in a reduced increase in biomass at the highest levels of fertilization (Isbell et al. 2013a). The increase in aboveground plant biomass can also affect fungal communities (Voříšková & Baldrian 2013), as more organic matter may increase fungal decomposer diversity (Cline et al. 2018). In turn, N retention decreases in highly intensified grassland soils as a result of higher N inputs and the dominance of fast-growing species with low root density (Ledgard et al. 2011; Kleinebecker et al. 2014). Our findings show that these well-known changes due to land use intensification may occur abruptly once a key threshold is crossed, which highlights the need to maintain low levels of land use to prevent rapid declines in diversity.
Thresholds associated with anthropogenic disturbance have been described for some ecosystems, such as eutrophicated lakes, and overgrazed drylands (Suding et al. 2004), but there had been little evidence for their importance in temperate grasslands (Sasaki et al.2015). Some previous studies have found abrupt changes in certain ecosystem-state variables in response to particular land use components (e.g. increasing grazing intensity changed vegetation composition; fertilization changed vegetation composition and soil properties) (Suding et al. 2005; Sasaki et al. 2008; Ramirez et al. 2010). In our analysis most changes in response to individual components were associated with the presence or absence of the component. It is well known that grazed and ungrazed or fertilized and unfertilized grasslands differ dramatically (Bai et al. 2010, 2012). However, our results also show thresholds in response to an integrated measure of land use intensity, suggesting that it is the combined effect of changes in multiple land use components that causes the abrupt changes in ecosystem states. Global change drivers usually operate synergistically by changing ecosystem feedbacks and leading to regime shifts that would not have happened if drivers acted individually (Suding et al. 2004; Briske et al. 2005; Rillig et al. 2019). Altogether, our results confirm the large impact that land use intensification has on ecosystems (Thébault et al. 2014; Newbold et al. 2015, 2016), while providing novel evidence for the existence of regime shifts in the diversity of aboveground primary producers and vertebrates, biomass production and nutrient retention in managed temperate grasslands.
Early warning signals at ecological thresholds
Early warning signals, such as increasing variability near a threshold, have been suggested as indicators of a system being about to switch between stable states (Scheffer & Carpenter 2003; Scheffer et al. 2009; Kéfi et al. 2014). Finding evidence for an increase in variance would therefore provide an indication that the thresholds we detected are associated with critical transitions. We found significant increases in variance for plants and some birds, suggesting they may experience a critical transition. However, several belowground variables also showed significant increases in variance but not a threshold response, which suggests that an increase in variance may not be a reliable early warning signal. Alternatively, it is possible that the abrupt transition in the plant community has cascading effects on other processes and changes their variance but not mean values. In grasslands, nutrient addition causes a shift from slow growing conservative, to fast growing acquisitive plant species, which is associated with increased productivity and faster soil nutrient cycling (Eskelinen et al.2020). At the transition between these two states there may be greater variability in plant functional composition between grasslands, which results in greater variability in various belowground processes. The existence of a critical transition between plant communities in managed grasslands would have important consequences. Extensively and intensively managed grasslands provide different ecosystem services, and a critical transition between these states would suggests that land use intensity needs to be kept well below the threshold in order to preserve the extensively managed, high-diversity state.
Hysteretic responses in the ecosystem
Our results showed that LUI thresholds for ecosystem functions can depend on whether land use recently increased or decreased, suggesting hysteretic dynamics. This hysteretic response indicates that returning to previous functioning levels requires lower land use intensity than is needed to change functioning as land use is intensified. Previous studies have suggested hysteretic dynamics in grasslands due to nutrient enrichment after fertilization (Isbell et al. 2013b), as nutrients can persist in the soil for many years (Hrevušová et al. 2009; Spohn et al. 2016). Thus, the slower recovery of nutrient retention, and slower decline in plant productivity, as land use is extensified may occur because fast-growing plants can maintain high dominance and productivity for some years after land use is reduced (Baeten et al. 2011). On the other hand, diversity thresholds were not affected by the direction of change in land use, suggesting a lack of hysteresis (Figure 4). This may be because diversity responds more slowly (Bommarco et al. 2014; Löffler et al. 2020). We only looked at whether land use intensity had increased or decreased relative to the previous year; however, if diversity responds more slowly than this, then only the long-term mean land use intensity on a plot may have an effect. We were not able to look at longer-term changes in land use as only 4% of plots experienced decreased, and 2% of plots increased, LUI for more than 5 consecutive years. Thus, although some studies have suggested that limited intensification can produce optimal biodiversity and functioning in grasslands (Yang et al. 2018), we do not find evidence for this. In our study area land use extensification (i.e. reducing fertilization while keeping high grazing or mowing levels) will not immediately reduce yield but it will also not support a rapid recovery of diversity. Our results therefore suggest that LUI needs to drop below 1 before high diversity grasslands could be promoted, i.e., no fertilization and low grazing or mowing. Finally, as abandonment of grassland management will lead to natural succession and the replacement of these semi-natural grasslands by shrubland and forests, extensive land practices are essential to preserve diverse grasslands (Queiroz et al. 2014). The existence of hysteresis associated with land use has key implications for conservation strategies, which further reinforces the idea that land use intensity needs to remain well below the threshold to preserve biodiversity.
Conclusions
We found evidence for thresholds in how land use intensification affects aboveground diversity and for a transition from extensively managed grasslands with high aboveground diversity and high soil nutrient retention, to intensively managed grasslands with high biomass production and belowground fungal diversity, but low aboveground diversity. Identifying these thresholds is key to prevent abrupt declines of biodiversity (LUI should not increase above 1) and to find the optimal, efficient management level allowing high productivity with lowest inputs (a LUI close to 2). In addition, extensively managed grasslands with land use levels below the threshold are priority targets for nature conservation, as it may be more difficult to restore grasslands once the threshold is crossed. Our results highlight the importance of testing for complex effects of global change drivers on multiple ecosystem components across many sites and multiple years to account for the high variability in responses that limit our capacity to identify thresholds (Hillebrand et al. 2020). As global change drivers can lead to critical transitions, it is important to anticipate them in order to avoid undesirable changes in both diversity and ecosystem functioning.
Acknowledgements
HS is supported by a María Zambrano fellowship funded by the Ministry of Universities and European Union-Next Generation plan. We thank the managers of the three Exploratories, K. Lorenzen, A. Hemp, S. Gockel, K. Wiesner, K. Wells and M. Gorke and all former and current managers for their work in maintaining the plot and project infrastructure; C. Fischer and V. Grießmeier for giving support through the central office, A. Ostrowski for managing the central data base, and E. Linsenmair, D. Hessenmöller, E.D. Schulze, W.W. Weisser and the late E. Kalko for their role in setting up the Biodiversity Exploratories project. We thank the administration of the Hainich national park, the UNESCO Biosphere Reserve Swabian Alb and the UNESCO Biosphere Reserve Schorfheide-Chorin as well as all land owners for the excellent collaboration. The work has been funded by the DFG Priority Program 1374 ”Biodiversity- Exploratories” (DFG-Refno.). Field work permits were issued by the responsible state environmental offices of Baden-Württemberg, Thüringen, and Brandenburg. We thank S. Soliveres for helping in the development of the ideas for this work and providing comments in late stages of the manuscript. We thank G. Prescott, A. Rindisbacher and N. Schenk for providing comments on the manuscript. We thank Sebastian Bischoff, Peter Escher, Martin Kaupenjohann, Katja Kerber, Beate Michalzik, Martin Schwarz, Jan Siemens, and Lisa Thieme of the project BECycles for their data contributions.
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Figure 1. Trajectories for regime shifts in ecosystems . Ecosystems experience a regime shift when they show a large change in an ecosystem state (i.e. variables describing the ecosystem) (a). This change can be due to one or more environmental drivers and can be gradual or fast, leading to multiple relationships (unbroken black line) between ecosystem state and environmental drivers. The regime shift can be gradual if the ecosystem state changes linearly with the driver (b), or abrupt if the change shows a threshold (c). In addition, thresholds can show hysteresis if the direction of the change (grey arrow) is associated with different thresholds (d). In this case, bringing the driver back across the original threshold will not return the ecosystem to its previous state (broken black lines).