Discussion
Our findings show that plant and soil biodiversity have
non-substitutable impacts on the temporal stability of community biomass
production. In the present study, soil biodiversity loss had a
detrimental effect on temporal stability by reducing the community-level
mean biomass production, increasing the temporal variability, and
weakening compensatory effects (via facilitation of uneven community
composition favoring grasses over herbs and legumes).
Consistent with previous studies
(Tilman et al. 2006; Hector et al. 2010; Hautier et
al. 2014; Hautier et al. 2015; Craven et al. 2018; Wanget al. 2019b), an increase in plant diversity in terms of both
species richness and functional diversity promoted temporal stability.
However, plant and soil biodiversity exerted independent effects on
temporal stability. Furthermore, when multitrophic biodiversity was
calculated from plant and soil biodiversity, multitrophic biodiversity
was positively and linearly associated with the temporal stability of
community biomass production. A large number of studies suggest that the
biodiversity of a single trophic group, e.g. the diversity of plants, is
a major factor stabilizing biomass production (Tilman et al.2006; Hector et al. 2010; Hautier et al. 2014; Hautieret al. 2015; Pennekamp et al. 2018; Craven et al.2018; Wang et al. 2019b). Our study suggests that maintaining
ecosystem functions (e.g. biomass production) when faced with
environmental variability requires biodiversity at multiple trophic
levels.
Compared with plant species richness, the diversity of plant functional
traits was a better explanatory
variable for temporal stability in diverse plant communities.
Exploitative plant species with fast-growing acquisitive traits, e.g.
high specific leaf area, leaf nitrogen concentration, specific root
length and specific root surface area, could recover rapidly following
disturbance, while conservative species with slow-growing traits, e.g.
low leaf dry matter concentration, high root average diameter and root
tissue density, may have a higher resistance to disturbance (Fischeret al. 2016; Liu et al. 2018; Mahaut et al. 2020;
Lozano et al. 2020; Freschet et al. 2020). Plant
communities with a higher diversity of functional traits likely imply a
stronger asynchronous response of plant species, e.g. a decrease in
exploitative plant species compensated by conservative species during
disturbance, and vice versa . In the present study, the diversity
of plant functional traits increased plant species asynchrony, and
subsequently, promoted the temporal stability of biomass production.
Plant species asynchrony is a main underlying mechanism by which plant
diversity stabilizes biomass production when faced with disturbance
(Loreau & de Mazancourt 2008; Isbell et al. 2009; Hectoret al. 2010; de Mazancourt et al. 2013; Loreau & de
Mazancourt 2013; Thibaut & Connolly 2013; Hautier et al. 2014;
Craven et al. 2018; Zhang et al. 2019). Supporting past
studies, we found that higher plant species richness, soil biodiversity
and multitrophic biodiversity promoted the temporal stability of biomass
production via enhancing plant species asynchrony. A previous study
found that the presence of natural soil biota
dramatically
increased the growth of legumes and herbs, and thus, promoted plant
species asynchrony under simulated environmental variation in
precipitation (Pellkofer et al. 2016). Our results suggest that
soil biodiversity is crucial for the occurrence of asynchrony of plant
species and particularly functional groups. In accordance with past
research (Wagg et al. 2014; Wagg et al. 2019; Prudentet al. 2020; Yang et al. 2020), we found that soil
biodiversity enhanced the performance of herbs and legumes during wet
and dry periods, likely indicating higher resistance during dry periods
or faster recovery during wet periods. Specifically, herbs had the
opportunity to recover from drought and differed from grasses in
response to the simulated variation in precipitation at high soil
biodiversity (Fig. 5). Besides, the dramatic reduction in legumes was
compensated by the rapid growth of grasses during the first drought
disturbance at high and moderate soil biodiversity. However, the
compensatory effect was weaker in low soil biodiversity because legumes
had already been suppressed by soil biodiversity loss before the first
drought disturbance. A recent study shows that soil biodiversity is more
important for herbs than grasses, and especially for the persistence of
legumes (Yang et al. 2020). Besides, the growth of herbs and
legumes is more reliable in the presence of mycorrhizal soil mutualists
(Hoeksema et al. 2010; van der Heijden et al. 2016). The
absence of these soil mutualists, in addition to the loss of soil
biodiversity, could have suppressed the performance of herbs and legumes
during and following drought in the present study.
It should be noted that soil biodiversity loss did not affect the growth
of herbs and grasses, and even increased the growth of legumes in the
monocultures. Therefore, soil biodiversity influenced the performance of
plant functional groups by regulating interactions among functional
groups in the mixed-species communities. For instance, soil biodiversity
increased the mean of plant community evenness by favouring herbs and
legumes. Although biodiversity can enhance the temporal stability by
promoting community evenness (Thibaut & Connolly 2013), we found that
plant community evenness was not related to the temporal stability of
community biomass production. Because the proportional abundance of
grasses was positively related to temporal stability, soil biodiversity
loss should increase temporal stability by promoting the dominance of
grasses. However, soil biodiversity loss exerted a negative effect on
temporal stability. Thus, the detrimental effect of soil biodiversity
loss on temporal stability cannot be directly attributed to its effect
on community evenness and the dominance of grasses, but can come from a
decrease in asynchrony of plant functional groups.
A decrease in population variance can also contribute to the temporal
stability of biomass production, because effects of treatments on
temporal stability can be decomposed into their effects on plant species
asynchrony and population variance (Thibaut & Connolly 2013). Higher
functional richness and soil biodiversity increased population variance,
which should decrease temporal stability. However, these detrimental
effects were neutralized by an increase in plant species asynchrony. An
increase in the temporal stability of biomass production can be caused
by both, an increase in the temporal mean of biomass production and a
reduction in the temporal standard deviation (Tilman et al. 2006;
Hautier et al. 2014). Consistent with most earlier studies
(Tilman et al. 2014; Hautier et al. 2014; Craven et
al. 2016; Weisser et al. 2017), our study supports the
hypothesis that an increase in plant species richness can promote
biomass production and decrease the temporal standard deviation of
biomass production.
Soil biodiversity loss can
decrease or increase biomass production, which depends on soil
biodiversity and soil community composition (Wagg et al. 2014).
Our results suggest that the temporal mean of biomass production was not
altered by soil biodiversity loss when monocultures were included, while
the temporal mean was decreased when monocultures were excluded (Fig. 3C
and H). This suggests that soil biodiversity loss has a detrimental
effect on the temporal mean of biomass production in diverse plant
communities. However, soil biodiversity loss did not affect plant
diversity-productivity relationships in diverse plant communities. Past
research shows soil pathogen suppression has more beneficial effects,
while the absence of soil mutualists exerts stronger detrimental effects
on biomass production in less diverse plant communities, and
consequently, influences plant diversity-productivity relationships
(Klironomos et al. 2000; Maron et al. 2011; Schnitzeret al. 2011; Luo et al. 2017; Liang et al. 2019;
Wang et al. 2019a). However, soil biodiversity loss did not alter
the strength of plant diversity effects on plant biomass production in
the present study. These results indicate that the effect of soil
biodiversity loss on plant productivity could not be simply due to the
loss of single soil pathogens or mutualists. In the present study, soil
biodiversity loss reduced plant fungal pathogens in soil inocula, and
reduced or even eliminated mycorrhizal soil mutualists in the phylum ofGlomeromycota at the last harvest. Reductions in soil pathogens
and mutualists have opposite effects on plant biomass production, and
therefore, effects of reductions in soil pathogens and mutualists along
soil biodiversity loss might cancel each other out. A decrease in plant
productivity could be caused by soil biodiversity loss in general other
than the loss of soil mutualists along with soil biodiversity loss
(Prudent et al. 2020; Yang et al. 2020).
Our study sheds new light on the
consequences of multitrophic biodiversity loss under global
anthropogenic change. Anthropogenic influences have been shown to
destabilize biomass production via reducing plant diversity (Hautieret al. 2015). Moreover, global
anthropogenic change, such as
nitrogen deposition, land-use intensification, warming, fertilization
and drought, can threaten both soil and plant biodiversity (Tsiafouliet al. 2015; Hautier et al. 2015; Gossner et al.2016; Banerjee et al. 2019; Geisen et al. 2019; Rilliget al. 2019; Zhou et al. 2020). Our study suggests that
the loss of multitrophic biodiversity could reduce the temporal
stability of biomass production by suppressing the occurrence of plant
species asynchrony or decreasing the mean of biomass production and
increasing its variation. These results indicate that the prediction of
biomass production under global anthropogenic change requires a
multitrophic evaluation of biodiversity loss.
In this study, the
dilution-to-extinction approach, which has been widely used to
investigate the relationships between rare soil microbial species and
ecosystem functions (Yan et al. 2015; Hol et al. 2015;
Roger et al. 2016; Maron et al. 2018; Domeignoz-Hortaet al. 2020), was employed to create a gradient of soil
biodiversity. Our results confirm that less abundant taxa were lost
first during dilution, followed by more abundant taxa (Yan et al.2015; Roger et al. 2016; Maron et al. 2018).
This
approach can simulate a realistic loss of soil biodiversity (Yanet al. 2015; Roger et al. 2016; Maron et al. 2018),
because less abundant taxa have a higher risk of extinction than
abundant species under anthropogenic changes (Zhou et al. 2020).
The present study used an open system, and an increase in bacterial
phyla was observed, compared to the initial soil inoculum. This means
that propagules from the environment contributed to soil biodiversity at
the last harvest. Contamination in a sterile treatment was even detected
in closed systems (Wagg et al. 2014) and is generally difficult
to avoid. Because soil biodiversity generally had a positive effect on
ecosystem functions in previous studies and our present study, this
indicates that we have underestimated the effect of soil biodiversity
loss on the temporal stability of biomass production.
In summary, our study suggests
that plant and soil biodiversity play non-substitutable roles in
stabilizing plant community biomass production. Although greater plant
diversity can promote the temporal stability of biomass production, the
reduction in temporal stability induced by soil biodiversity loss cannot
be compensated via increasing plant diversity. This result highlights
the significance of multitrophic biodiversity for stabilizing ecosystem
functions. Our study has important implications for restoration and
conservation management in terrestrial ecosystems. First, it is
important to preserve biodiversity at multiple trophic levels to
stabilize ecosystem functions, especially in ecosystems suffering from
intense disturbance. Second, although biomass production can be
stabilized via increasing plant diversity by restoration or conservation
measures, we should not ignore the importance of maintaining soil
biodiversity, since low levels of soil biodiversity can destabilize
biomass production.