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).