Content uploaded by Shuli Niu
Author content
All content in this area was uploaded by Shuli Niu on Feb 28, 2023
Content may be subject to copyright.
Common Species Stability
and Species Asynchrony Rather
than Richness Determine Ecosystem
Stability Under Nitrogen Enrichment
Fangfang Ma,
1,2
Fangyue Zhang,
1,2
Quan Quan,
1,2
Bing Song,
1,2
Jinsong Wang,
1
Qingping Zhou,
3
and Shuli Niu
1,2
*
1
Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research,
Chinese Academy of Sciences, Beijing 100101, China;
2
Department of Resources and Environment, University of Chinese Academy of
Sciences, Beijing 100049, China;
3
Institute of Qinghai-Tibetan Plateau, Southwest University for Nationalities, Chengdu 610041,
China
ABSTRACT
Global nitrogen (N) deposition generally reduces
ecosystem stability. However, less is known about the
responses of ecosystem stability and its driving
mechanisms under different N addition gradients. We
conducted a four-year N addition experiment in an
alpine meadow, using six levels of N addition rates (0,
2, 4, 8, 16, 32 g N m
-2
year
-1
) to examine the effects
of N addition on plant community biomass stability
and the underlying mechanisms. We found that the
stability of ecosystem aboveground net primary pro-
ductivity (ANPP) decreased linearly with increasing N
addition rates, even though it had no effect on plant
speciesrichnessatlowNadditionratesandsignifi-
cantly reduced species richness at high N addition
rates.Themostremarkablefindingisthatthemain
mechanism underlying ecosystem stability shifted
with N addition rates. The decrease of common species
stability contributed most to the reduction of plant
community biomass stability under low N addition
rates (N0–N4), whereas the decrease of species asyn-
chrony contributed most to the reducing plant com-
munity biomass stability under high N addition rates
(N8–N32). Our results indicate that species diversity
was not a significant predictor of plant community
biomass stability in this alpine meadow, which chal-
lenges the traditional knowledge. This study high-
lights the shifts of main mechanism regulating plant
community biomass stability under different N addi-
tion rates, and suggests that continuous nitrogen
deposition in the future may reduce ecosystem sta-
bility and potentially impeding the sustainable provi-
sion of ecosystem functions and services.
Key words: Common species stability; Dominant
species stability; Ecosystem stability; N addition;
Species asynchrony; Species richness.
Received 14 April 2020; accepted 1 August 2020
Electronic supplementary material: The online version of this article
(https://doi.org/10.1007/s10021-020-00543-2) contains supplementary
material, which is available to authorized users.
Authors Contributions NSL and MFF conceived the ideas and de-
signed the experiment; MFF, ZFY, QQ, SB, WJS and ZQP conducted the
field experiment and analyzed the data; MFF led the writing of the
manuscript. All authors contributed critically to the drafts and gave final
approval for publication.
*Corresponding author; e-mail: sniu@igsnrr.ac.cn
Ecosystems
https://doi.org/10.1007/s10021-020-00543-2
2020 Springer Science+Business Media, LLC, part of Springer Nature
HIGHLIGHTS
Ecosystem stability decreased linearly with
increasing N addition rates.
Species diversity was not a significant predictor
of community biomass stability.
The main mechanism underlying ecosystem sta-
bility shifted with N addition rates.
INTRODUCTION
Ecosystem stability is crucial for the provision of
ecosystem functions and services, as it refers to the
ability of ecosystems to maintain consistent inter-
annual productivity in changing environment
(Tilman and others 2001; Isbell and others 2015;
Oliver and others 2015). Much effort has been
devoted to studying the characteristics and poten-
tial mechanisms of the stability of ecosystem pro-
ductivity under the background that many
ecosystems are experiencing striking human-in-
duced environmental changes (Grman and others
2010; Loreau and de Mazancourt 2013; Hautier
and others 2015). And evidence is accumulating
that plant species biodiversity is the principal factor
determining the stability of ecosystem productivity
(Tilman and others 2006; Loreau and de Mazan-
court 2013; Hautier and others 2015). The pro-
moting effects of species diversity on ecosystem
stability are mainly through mechanisms such as
the sampling effect (Loreau and Hector 2001), the
compensatory effect (Loreau and de Mazancourt
2008; Allan and others 2011), and the portfolio
effect (Tilman and others 2006). Higher species
diversity would increase the probability to include
species that are resistant to environmental distur-
bance or better adapt to the changing environment
(the sampling effect) (Loreau and Hector 2001;
Polley and others 2003). The compensatory effect
states that niche differentiation among species al-
low them to capture resources in ways that are
complementary in space or time, allowing
stable multispecies coexistence (Mulder and others
2001; Cardinale and others 2007). As a main form
of temporal niche differentiation, species asyn-
chrony is expected to promote ecosystem stability
(Grman and others 2010). Species asynchrony re-
fers to a reduction in the abundance of one species
is more likely to be compensated by the increase in
the abundance of other species (Keitt 2008; Loreau
and de Mazancourt 2008), mainly through the
discordant responses of species with distinct func-
tional traits to environmental fluctuations and
interspecific competition (Adler and others 2013;
Loreau and de Mazancourt 2013; Leps and others
2018). As another mechanism for stabilizing
ecosystem functions, the mean–variance scaling
relationship (the portfolio effect), which empha-
sizes the statistical averaging effect of multiple
species (Cottingham and others 2001), indicates
that the higher species richness, the more likely the
variance of a community is to be lower than the
additive variance of constituent species, ultimately
making the community more stable (Doak and
others 1998; van Ruijven and Berendse 2007).
Furthermore, a growing body of studies support
the mass ratio hypothesis proposed by Grime (Ma
and others 2017; Yang and others 2017), which
predicted that ecosystem attributes are mainly
determined by the characteristics of dominants
(Grime 1998), so the stability of dominant species
contributes largely to the ecosystem stability to a
large extent (Zelikova and others 2014; Ma and
others 2017). In some circumstances, the dynamics
of dominant plants may also constrain the gener-
ality of diversity-stability relationships (Steiner and
others 2005; Wayne Polley and others 2007).
Subordinate and/or rare species may also con-
tribute largely to ecosystem stability if their pres-
ence promotes feeble trophic interactions (Jiang
and Pu 2009; Downing and others 2014; Yang and
others 2017). Hence, global changes that affect
species diversity, species asynchrony and the
dominant species stability have consequences
potentially for ecosystem stability (Ma and others
2017).
As a major manifestation of global change,
anthropogenic reactive nitrogen (N) has increased
more than threefold over the last century and is
projected to further raise dramatically in coming
decades (Galloway and others 2004; Galloway and
others 2008). Mounting evidence indicates that
nitrogen enrichment is a serious threat to species
diversity, and likely to profoundly affect ecosystem
functioning and services (Bai and others 2010;
Zhang and others 2014; Stevens and others 2015).
For example, sustained stress of nitrogen fertiliza-
tion in grassland communities typically reduces
species richness (Suding and others 2005; Zhang
and others 2014), shifts species distribution and
dominance (Hillebrand and others 2008; Gonzalez
and Loreau 2009), increases synchrony among
constituent species (Hautier and others 2014;
Zhang and others 2016), which in turn can have a
profoundly negative effect on ecosystem stability
(Yang and others 2012). However, some other
studies demonstrated that N addition has no affect
(Leps 2004; Grman and others 2010) or even in-
F. Ma and others
creases ecosystem stability in the long term (Steiner
and others 2005; Yang and others 2011c). And the
relative contribution of mechanisms affecting
ecosystem stability is also contentious in different
terrestrial ecosystems (Grman and others 2010;
Zhang and others 2017). Accordingly, the re-
sponses of stability of ecosystem productivity to N
addition and the main mechanisms are still con-
troversial and poorly understood. And the dis-
crepancy among different studies invites more
empirical evidence to address the long-standing
topic. Moreover, many previous studies on the ef-
fects of nitrogen addition on ecosystem function
mainly focus on a single addition rate (Stevens and
others 2015; Zhao and others 2019; Wu and others
2020), which is considered to be highly uncertain
for the accurate prediction of ecosystem functions
(Gomez-Casanovas and others 2016). Seeing that
the impact of N addition on biodiversity and
ecosystem aboveground net primary productivity
(ANPP) is dose-dependent (Humbert and others
2016; Ma and others 2020), the positive diversity-
stability relationships (Hector and others 2010;
Yang and others 2012) and the key drivers of ANPP
responses to N enrichment vary with N addition
rate (Ma and others 2020), we hypothesized that
the intensity of N effect on plant community bio-
mass stability is determined by N addition rate. In
addition, the relative contributions of stabilizing
mechanisms vary also with nitrogen addition rates.
In this study, we investigated the responses of
plant community biomass stability to a N addition
gradient using a manipulative experiment in an
alpine meadow on the Tibetan Plateau (Song and
others 2017; Ma and others 2018; Ma and others
2020). Being the earth’s third pole and the largest
plateau in the world, the Tibetan Plateau
(>4000 m a.s.l.) is vulnerable to human activities
and climate change, and has been undergoing an
evident increase in N deposition from 0.87 to
1.38 g N m
-2
year
-1
(Lu
¨and Tian 2007). The un-
ique geographical location and climatic character-
istics of the Tibetan Plateau call for a pressing
understanding concerning how ecosystem stability
changes under increasing N addition rates. This will
promote the sustainable provision of grassland
ecosystem functions and services and will have
profound implications for the global carbon bal-
ance. Particularly, we aim to answer the following
questions: (1) how community biomass stability
responded to different N addition rates? (2) which
mechanism governed the effects of N fertilization
on plant community biomass stability? (3) whether
and how the key mechanisms of plant community
biomass stability shift with nitrogen addition rate?
MATERIALS AND METHODS
Study Site
This field experiment was implemented in an al-
pine meadow (3500 m a.s.l.) located at the eastern
Qinghai-Tibetan Plateau (3248N, 10233E) in
Hongyuan County, Sichuan province, China.
Long-term (1961–2013) mean annual precipitation
and mean annual temperature are 747 mm and
1.5 C, respectively. On the basis of Chinese clas-
sification, the soil at this research site is classified as
Mat Cry-gelic Cambisol (Li and Sun, 2011). The soil
total C and N content are 37 g C kg
-1
and
3.5 g N kg
-1
, respectively. The pH is 6.24 ±0.09.
This experimental site was dominated by grass
(Deschampsia caespitosa (Linn.) Beauv.), sedge
(Carex) and forbs (Polygonum viviparum L.,
Euphorbia esula Linn., and Anemone trullifolia
var. linearis (Bruhl) Hand.-Mazz.).
Experimental Design
This N addition experiment with six levels of N
addition rate (0, 2, 4, 8, 16, 32 g N m
-2
year
-1
) was
started in early May 2014, following a complete
random block design. Each treatment was repeated
randomly five times, causing 30 plots of 8 98m
totally, and any two adjacent plots were 3 m apart.
During the growing season (May–September) of
2014–2018, N was applied as NH
4
NO
3
(>99%) by
hand every month before rainfall. Soil inorganic
nitrogen (SIN) increased gradually with the
increasing N addition rate (linear mixed-effects
model: P<0.001; Supplementary Fig. 8), which
indicated that the expected treatment effect had
been achieved. The detailed experimental design
has also been presented in Song and others (2017)
and Ma and others (2018).
ANPP Measurement
Aboveground net primary productivity (ANPP) was
sampled during the peak biomass period (usually
between 10 and 15 August) of 2015–2018. All the
aboveground parts of plants were cut off at the
ground level in a quadrat frame (0.50 90.50 m),
which was randomly placed in each plot. All living
plants were separated into species and oven-dried
at 65 C for 48 h until they reach a constant weight
and weighed.
Common Species Stability and Species Asynchrony Rather than Richness
Statistical Analysis
Temporal stability of plant community biomass in
each plot was quantified as the ratio of temporal
mean ANPP (l) to its standard deviation (r) across
the years 2015–2018 (Zhang and others 2016;Ma
and others 2017; Sasaki and others 2019). The
temporal stability of population and groups (dom-
inant, common and rare) were calculated using the
same method over the 4 years (2015 to 2018).
Species diversity in each plot was estimated by
species richness, which was defined as the total
number of species appeared in the same frame that
above ground net primary productivity was sam-
pled every year, and Simpson’s dominance index,
which was calculated as follows:
Simpson ¼X
n
i¼1
bi
B
2
where iis the number of species in the sample,
1£i£n. biis the biomass of species i, and Bis the
ecosystem biomass in a plot with nspecies (Leps
2004).
To ascertain whether species diversity enhances
ecosystem stability through the mean–variance
scaling and whether N addition would affect the
mean–variance scaling, we examined the mean–
variance scaling relationship (Taylor’s power law)
on ecosystem biomass stability. The relationship
was described as:
r2¼cmz
where r
2
is the variance in ANPP per species, c is a
constant, m is the average ANPP per species, and z
is the scaling coefficient. When 1 <z<2, diver-
sity is expected to enhance plant community bio-
mass stability via the mean–variance scaling
(Tilman and others 1998; Grman and others 2010).
Species asynchrony was quantified as:
uy¼1ux¼1
r2
Pn
i¼1ri
2
where uyis species asynchrony of each plot, uxis
species synchrony of each plot, r
2
is the variance of
plant community biomass and r
i
is the standard
deviation of biomass of species iin a plot with n
species (Loreau and de Mazancourt 2008; Ma and
others 2017). This index attains one when species
fluctuations are perfectly asynchronized, and at-
tains zero when species fluctuations are perfectly
synchronized (Ma and others 2017).
Based on their average relative abundance
throughout the study period (2015–2018), plants
were further divided into three species groups,
dominant (>5%), common (1 5%) and rare
(<1%) species (Chen and others 2016; Ma and
others 2017). The three species groups consisted of
5, 14 and 26 species, and accounted for 61.53%,
33.78%, and 4.69% of plant community biomass,
respectively (Supplementary Table 4). Because
there was no significant difference between species
richness under N2-N4 and that under the control,
but species richness under N8-N32 treatment was
significantly lower than that under control (Fig-
ure 2A), thus the mechanisms of plant community
biomass stability were explored for the three N
addition levels: low N addition rates (N0–N4), high
N addition rates (N8–N32) and total N addition
rates (N0–N32).
Linear mixed-effects models were performed to
assess the effects of N addition on plant community
biomass temporal stability, species asynchrony, the
stability of the three different abundance groups
(dominant, common and rare species), in which N
addition was treated as a fixed factor, and block was
treated as a random factor. The LSD test (p<0.05)
was used for a posteriori comparisons. Linear
mixed-effects models were also performed to
examine the effects of N addition, year and their
interaction on ANPP, species richness, and species
dominance, in which N addition and year were
treated as fixed factors, and block was treated as a
random factor. All statistical analyses were con-
ducted using SPSS 22.0 software (SPSS Inc. 2004).
We conducted linear regressions to evaluate the
relationships between log (species variance of bio-
mass) and log (species mean biomass) for different
N addition treatments, and ANCOVA was used to
test the difference of the slopes of the linear
regressions. We used regression analysis to explore
relationships between plant community biomass
stability and species dominance, species asyn-
chrony, species richness, and the stability of dom-
inant, common and rare species. According to the
regression results, we further calculated dominant
species asynchrony and common species asyn-
chrony to explore their effects on plant community
biomass and dominant/common species stability.
Based on our regression results, structural
equation model (SEM) was performed to explore
the pathways of how N addition affected plant
community biomass stability through species rich-
ness, species asynchrony, species dominance,
dominant species stability and common species
stability for the three N addition levels (N0–N4, N8–
N32 and N0–N32). We first considered a full model
that included all possible pathways (Supplemen-
tary Fig. 1), and the fit of final model was evaluated
using the v
2
test, root square mean errors of
F. Ma and others
approximation (RMSEA) and Akaike information
criteria (AIC). The criteria for determining the final
model was as follows. First, the P value of the
structural equation model should be greater than
0.05 (excluding M1, M3, M4 and M7, Supple-
mentary Table 5). Second, we selected the models
with smaller AIC value, which indicates better
goodness-of-fit (only M2 had the lowest AIC under
N0–N32, N0–N4 and N8–N32 treatments). Third,
based on the first two criteria, we finally selected
the models with smaller v
2
and RMSEA values. All
statistical analyses were conducted with SPSS 22.0
software (SPSS Inc., 2004). The SEM analyses were
performed using AMOS 21.0 (Amos Development
Corporation, Chicago, IL, USA). Origin 8.5 was
used for plotting data.
RESULTS
Plant Community Biomass and its
Stability in Response to N Addition
Gradient
Over the 4-year experimental period, N addition
had significant effects on plant community biomass
stability (linear mixed-effects model: P= 0.008;
Figure 1A), ANPP (linear mixed-effects model:
P= 0.023; Figure 1B), and species richness (linear
mixed-effects model: P= 0.008; Figure 2A). With
the increasing N addition rates, community stabil-
ity decreased linearly, but ANPP and species rich-
ness showed a unimodal response. The largest
value of community stability was 5.75 ±0.81 un-
der 2 gN m
-2
year
-1
addition rate (N2), and sig-
nificantly improved by 63.04% and 114.08%
compared with N16 and N32 (Figure 1A), respec-
tively. The highest value of ANPP was
428.96 ±28.94 under 4 gN m
-2
year
-1
addition
rate (N4), and significantly increased by 23.66%,
16.66% and 13.01% on average compared with the
control, N2 and N32 (Figure 1B), respectively. The
largest value of species richness was 22 ±1 under 2
gN m
-2
year
-1
addition rate (N2), and there was no
significant difference in species richness between
the control (N0) and N2 or N4, but the species
richness under N8, N16 and N32 was significantly
lower than that of the control (N0) (Figure 2A).
However, species dominance increased gradually
with the increasing N addition rate (linear mixed-
effects model: P<0.001; Figure 2B). With the
increasing N addition rates, the biomass of grasses
and sedges increased, whereas that of legumes and
forbs decreased (Supplementary Fig. 6a). The lost
species mainly included Geum aleppicum Jacq.,
Halenia elliptica D. Don var. elliptica,Gentianopsis
paludosa (Hook. f.) Ma,Cerastium arvense Linn., and
Anaphalis lacteal (Supplementary Fig. 6b).
The Response of Compensatory
Dynamics and Group Stability to N
Addition
Species asynchrony decreased linearly with the
increasing N addition rate, and the species asyn-
chrony under N32 was significantly lower by
11.19%, 11.94%, 9.98%, and 7.59% than that
under the control (N0), N2, N4 and N8, respec-
tively (P= 0.012; Figure 2C and Supplementary
Table 1). The stability of different species groups
(dominant, common and rare) responded differ-
ently to the increasing N addition rate. The domi-
nant species stability showed a saturated response
with the increasing N addition rate, and the dom-
inant species stability under N2 was significantly
higher by 53.92% and 54.28% than that under
Figure 1. Community biomass stability (A) and aboveground net primary production (ANPP) (B) in response to N
addition gradients. Mean ±se. The values of community stability and ANPP under each nitrogen addition treatment are
an average of 4 years (2015–2018). Different letters indicate significant difference at P <0.05.
Common Species Stability and Species Asynchrony Rather than Richness
N16 and N32 (Figure 2D), respectively. The re-
sponse patterns of the common species stability and
rare species stability were similar to that of domi-
nant species stability. N addition had a significant
effect on the common species stability (P= 0.001;
Figure 2E and Supplementary Table 1), but no
significant difference was found between rare spe-
cies stability under different N addition rates
(P= 0.367; Figure 2F and Supplementary Table 1).
Bivariate regressions showed that plant com-
munity biomass stability significantly increased
with increasing species richness (Figure 3A,
R
2
= 0.33, P<0.001), species asynchrony (Fig-
ure 3B, R
2
= 0.60, P<0.001), and significantly
decreased with increasing species dominance (Fig-
ure 3C, R
2
= 0.11, P<0.05). Dominant species
stability (Figure 3D, R
2
= 0.31, P<0.001), com-
mon species stability (Figure 3E, R
2
= 0.23,
P<0.01) and population stability (Supplementary
Fig. 7a, R
2
= 0.15, P<0.05) promoted ANPP sta-
bility significantly. There was no relationship be-
tween plant community biomass stability and rare
species stability (Figure 3F). Population stability
significantly increased with increasing species
richness (Supplementary Fig. 7b, R
2
= 0.11,
P<0.05), whereas the standard deviation of ANPP
(Supplementary Fig. 5, R
2
= 0.27, P<0.01) sig-
nificantly decreased.
Effects of N Addition on Mean–Variance
Scaling
Log-transformed values of the variance of species
ANPP were positively correlated to the log-trans-
formed values of its mean in all six N addition
Figure 2. Species richness (A), species dominance (B), species asynchrony (C), dominant species stability (D), common
species stability (E), and rare species stability (F) in response to N addition gradients. Mean ±se. The values of all indexes
under each nitrogen addition treatment are an average of 4 years (2015–2018). Different letters indicate significant
difference at P<0.05.
F. Ma and others
treatments (Figure 4; all P<0.001). The scaling
coefficients z (slopes) for the six N addition treat-
ments from N0 to N32 were 1.76, 1.73, 1.73, 1.68,
1.82 and 1.77, respectively, indicating that species
richness could promote the plant community bio-
mass stability via the mean–variance scaling in all
treatments. However, N addition did not alter the
scaling coefficient z (Supplementary Table 3).
The Impact Pathways of the N Addition
Effect on Community Biomass Stability
N addition had negative effects on plant commu-
nity biomass stability, but the impact pathways
were different between low versus high N addition
rates. Under N0–N4 treatment, the total effect of N
addition on plant community biomass stability was
negative, with the standardized total effect size
being -0.078 (Figure 5, Supplementary Table 2).
The negative effect of N addition on plant com-
munity biomass stability was mainly through its
negative effect on common species stability (path
coefficients = -0.47, Figure 5, Supplementary
Table 2, P<0.05). Common species stability had
significantly positive correlation with common
Figure 3. Relationships between ecological factors and ANPP stability. Shown are (A) species richness (linear regression;
P<0.001); (B) species asynchrony (linear regression; P<0.001); (C) species dominance (linear regression; P<0.05);
(D) dominant species asynchrony (linear regression; P<0.001); (E) common species stability (linear regression;
P<0.01); and (F) rare species stability. The black solid lines are significant regression lines. Each orange hollow circle
represents an experimental plot (n= 30). Shaded area represents 95% confidence intervals.
Figure 4. Relationships between the logarithm of
variance in above ground net primary production
(ANPP) and the logarithm of the mean biomass per
0.25 m
2
sampling area for each species.
Common Species Stability and Species Asynchrony Rather than Richness
species asynchrony (R
2
= 0.50, P<0.001, Sup-
plementary Fig. 3). The SEM model explained 64%
of the variation in plant community biomass sta-
bility. Under N8–N32 treatment, the total effect of
N addition on plant community biomass stability
was negative too, with the standardized total effect
size being -0.55 (Figure 5, Supplementary Ta-
ble 2). The negative effect of N addition on plant
community biomass stability was mainly through
its negative effect on species asynchrony (path
coefficient = -0.52, P<0.05, Figure 5). The SEM
model explained 80% of the variation in plant
Figure 5. The results of structural equation model (SEM) analysis showing the effect of N addition on community biomass
stability via pathways of dominance, richness, species asynchrony, stability of dominant and common species. Red and
blue solid arrows represent significant positive and negative pathways, respectively, grey dashed arrows indicate
nonsignificant pathways. The R
2
values associated with variables indicate the proportion of variance explained by
relationships with other variables. The values adjacent to arrows are standardized path coefficients which reflect the effect
size of the relationship. Arrow width is proportional to the strength of the relationship. Goodness-of-fit statistics for low-
level N addition (N0–N4): v
2
= 9.240, P= 0.509, d.f. = 10; root mean square error of approximation (RMSEA) <0.001,
AIC = 45.24, and for high-level warming (N8–N32): v
2
= 10.868, P= 0.368, d.f. = 10; RMSEA = 0.08; AIC = 46.87.
Significant level: ***P<0.001; **P<0.01; *P<0.05.
F. Ma and others
community biomass stability. Thus the total effects
of N addition on plant community biomass stability
were negative under N0–N32 (Supplementary
Fig. 2 and Table 2), and 80% of the variation in
plant community biomass stability was mainly ex-
plained by species asynchrony and dominant spe-
cies stability (Supplementary Fig. 2). The dominant
species stability correlated positively with domi-
nant species asynchrony (R
2
= 0.12, P<0.05,
Supplementary Fig. 3). In regression analyses,
species richness showed positive association with
plant community biomass stability (Figure 3A) and
species asynchrony (Supplementary Fig. 4a). In
SEM, note that species richness was excluded from
SEM as a significant predictor of plant community
biomass stability (Figure 5).
DISCUSSION
Little Contribution of Species Richness
on Ecosystem Stability Under N
Enrichment
The species richness decreased significantly only
under high nitrogen addition rates (N8–N32),
indicating that the effects of N addition on plant
diversity depend on the N addition rates, which is
similar with Humbert and others (2016). More-
over, with the increasing N addition rates, the plant
community biomass stability decreased gradually in
our study (Figure 1A). According to the definition
of temporal stability of plant community biomass
(Ma and others 2017; Sasaki and others 2019), a
decrease in ecosystem stability is mainly due to a
decrease in the mean relative to the standard
deviation of ANPP (Hautier and others 2014; Zhang
and others 2016). In our study, the decrease of
ecosystem stability caused by N addition was
mainly due to the increase of standard deviation of
ANPP (Supplementary Fig. 5). The result that N
addition weakens ecosystem stability is consistent
with previous studies (Yang and others 2012;
Hautier and others 2014; Zhang and others 2016),
and supports our hypothesis that the response of
ecosystem stability to nitrogen addition depends on
N addition rates. However, the linear decrease of
stability with N addition rate is in contrast with Niu
and others (2018) and Romanuk and others
(2006), who pointed out that the response of
community stability to N enrichment is nonlinear
(Romanuk and others 2006; Niu and others 2018).
This might be attributed to differences in nitrogen
addition dose, application duration, climate and
vegetation types at the study area (Humbert and
others 2016; Niu and others 2018).
Many previous studies, including theoretical
models (Cardinale and others 2013; Loreau and de
Mazancourt 2013), laboratory experiments (Tilman
and others 2006; Wright and others 2015) and field
observations (Romanuk and others 2006; Jiang and
Pu 2009), demonstrated that greater species diver-
sity contributes to higher plant community biomass
stability. Contrary to this traditional knowledge,
however, species richness was not the determinant
factor for ecosystem stability in our study (Fig-
ure 5). This may be mainly due to the following
reasons. First, species richness only changed
(gained or lost) by 1 2 species per 0.25 m
2
under
low nitrogen addition rates (N2–N4, Figure 2A),
which is a very small variation for the alpine
meadow with abundant species per 0.25 m
2
(19–22
species). So it is not surprising that species richness
has a small impact on the plant community bio-
mass stability under low N addition rates. Second,
most of the lost species under high N addition rates
were rare species (Supplementary Fig. 6b),
including Geum aleppicum Jacq.,Halenia elliptica D.
Don var. elliptica,Gentianopsis paludosa (Hook. f.) Ma,
Cerastium arvense Linn., and Anaphalis lacteal, which
accounted for only a small part of the plant com-
munity biomass (Supplementary Table 4) and the
rare species stability was lower than that of domi-
nant and common species stability (Figure 2D–F).
Third, the coexistence of other stabilizing mecha-
nisms of species diversity on plant community
biomass stability overrides the significant influence
of species richness on plant community biomass
stability (Jiang and Pu 2009).
Those other stabilizing mechanisms include the
following aspects. The first one is species asyn-
chrony. Studies have suggested that fertilization
might make species more vulnerable to environ-
mental fluctuations or more strongly competing
(Grman and others 2010). So the strength of spe-
cies asynchrony on the ecosystem stability under N
enrichment may be stronger than the species
richness (Figure 5), leading to the concealment of
the significant impact of species richness on
ecosystem stability in the SEM. The second one is
the regulation of population-level stability. In our
study, N-induced decline of plant community bio-
mass stability was partly due to a decrease in pop-
ulation stability (Supplementary Fig. 7). This is in
concert with Valone and Hoffman (2003), who
suggests that population stability overrides poten-
tial effects of diversity to some extent (Valone and
Hoffman, 2003). Third, as a ubiquitous stabilizing
mechanism of communities, the mean–variance
scaling describes the phenomenon where a com-
munity with more species is more likely to lower its
Common Species Stability and Species Asynchrony Rather than Richness
variation in ecosystem properties through statistical
averaging (Doak and others 1998), and the slope of
the scaling relationship zdetermines the strength of
this stabilizing mechanism, as summarized by
Taylor’s power law (Grman and others 2010).
When 2 >z>1, the mean–variance scaling
relationship (The portfolio effect) indicates that
diversity is expected to increase ecosystem stability
(Tilman and others 1998). In our study, the slopes z
of all nitrogen addition treatments were between 1
and 2 (Figure 4), but there was no significant dif-
ference between the zvalues of different nitrogen
addition treatments and the control (Supplemen-
tary Table 3). This result indicates that as one of the
underlying mechanisms of positive effects of spe-
cies richness on plant community biomass stability,
the mean–variance relationships in our study did
not contribute to a decrease in plant community
biomass stability under the condition of N-induced
species richness loss. And the conclusion that spe-
cies dominance increased gradually with the
increasing N addition rates further determined that
the mean–variance scaling is not important in this
alpine meadow (Figure 2B), because the portfolio
effects are particularly important when biomass is
equally distributed among species (higher species
evenness) (Hillebrand and others 2008; Grman and
others 2010).
The Mechanisms Underlying Community
Biomass Stability Vary with N Addition
Rates
Notably, we found that the key drivers affecting
temporal stability of plant community biomass
shifted with N addition rates (Figure 5). The
transformation of the key mechanisms in regulat-
ing ecosystem stability may be caused by the dif-
ferential response of species richness to N addition
in the low and high N addition rates. Dominant
species stability is one of the most crucial contri-
bution to plant community biomass stability from
N0–N32 in our study (Supplementary Fig. 2),
indicating the important role of dominant species
stability in determining ecosystem stability (Grman
and others 2010; Yang and others 2011b; Wilsey
and others 2014). In our experiment, the five
dominant species, Deschampsia caespitosa (Linn.)
Beauv, Polygonum viviparum L, Euphorbia esula Linn,
Carex and Cremanthodium lineare Maxim, accounted
for approximately two-thirds (61.53%) of plant
community biomass. Similar to the concept of
sampling effect, the stabilizing effect of dominant
species stability on plant community biomass stems
from the predominant contribution of dominant
species to ecosystem functioning (Tilman, 1999;
Yang and others 2017). Common species repre-
sented 31.11% of species richness, they accounted
for 33.78% of plant community biomass. Rare
species represented 57.78% of species richness, but
they only accounted for 4.69% of plant community
biomass (Supplementary Table 4). As a result,
there was no significant relationship between plant
community biomass stability and rare species sta-
bility in our experiment (Figure 3F), but there is a
significant relationship between the common spe-
cies stability and plant community biomass stability
(Figure 3E).
More interestingly, common species stability is
the main mechanism leading to the decrease of
plant community biomass stability under low N
addition rates (N0–N4, Figure 5), which is caused
by reducing common species asynchrony (Supple-
mentary Fig. 3d). This is mainly because that the
alleviation of N limitation under increasing N
addition rates might modify the dominance hier-
archy of this studied ecosystem and increase the
abundance of common species (Sasaki and Lauen-
roth 2011). This result also suggests that the effects
of common species on ecosystem stability are
strengthened at low N addition rates. Therefore,
neglecting the potential contribution of common
species could lead to a biased understanding of the
key drivers of ecosystem stability in the context of
global change (Downing and others 2014).
In high N addition rates (N8–N32), N addition
reduced species richness significantly (Figure 2A),
and further species asynchrony which was the
main driver in regulating ecosystem stability (Fig-
ure 2C), because of the positive species richness-
species asynchrony relationship (Supplementary
Fig. 4a, R
2
= 0.30, P<0.01). Furthermore, species
asynchrony was identified as a principal contribu-
tor of plant community biomass stability under
high N addition rates. This is congruent with a
variety of empirical studies (Zhang and others
2016; Zhang and others 2019). As the leading
mechanism contributing to the decrease of plant
community biomass stability under high N addition
rates, the decrease of species asynchrony under
nitrogen enrichment is mainly caused by the fol-
lowing reasons. First, N addition usually promotes
the growth of grasses and sedges species but causes
the disappearance of leguminous species (Supple-
mentary Fig. 6a). Although grasses and sedges are
always higher in height to suppress light in other
plants (Niu and others 2010; Song and others 2012)
and able to quickly explore available resources
(Yang and others 2011a). This means that N
enrichment makes species oscillate more syn-
F. Ma and others
chronously in this alpine meadow, decreases spe-
cies asynchrony and consequently reduces ecosys-
tem stability. Moreover, as suggested by stress-
gradient hypothesis, the relative strength of com-
petition-facilitation among species are often envi-
ronmentally contextualized (Callaway and Walker
1997; Callaway and others 2002), facilitation
would outweigh competition in harsh environ-
mental conditions (Callaway and others 2002; Yang
and others 2016), allowing species to respond in a
more synchronized manner to high N addition
rates, because N enrichment caused soil acidifica-
tion and ammonium toxicity in this alpine meadow
(Ma and others 2020), ultimately reducing
ecosystem stability. Probably more important, as
suggested by Dijkstra and others (2018) that species
asynchrony was positively correlated with com-
munity N turnover, high N addition with signifi-
cantly increased soil inorganic nitrogen content
(Supplementary Fig. 8) might reduce community N
turnover and in turn reduce species asynchrony
and plant community biomass stability, making
species asynchrony contribute most to plant com-
munity biomass stability under high nitrogen
addition rate (Dijkstra and others 2018). So our
results indicate that the main mechanism under-
lying ecosystem stability shifted from common
species stability at low N addition to species asyn-
chrony at high N addition rates, which reconciles
the conflicting conclusions in previous studies
using only one N addition rate.
CONCLUSIONS
Based on a field N addition gradient experiment,
this study explored the responses of ecosystem
stability to increasing N addition rates and found
that plant community biomass stability decreased
linearly with the increasing N addition rates. The
mechanism underlying the decreased stability var-
ied with N addition rates. Under low N addition
rates (N0–N4), changes in common species stability
contributed most to the plant community biomass
stability. But species asynchrony became the
dominant mechanism affecting the plant commu-
nity biomass stability at high N addition rates. This
result challenges the traditional conclusion that
higher community biomass stability is mainly due
to higher species richness. Our study demonstrates
the importance of considering the shifting mecha-
nisms when predicting the effects of global N
deposition on ecosystem stability. This results will
also provide a theoretical basis for achieving sus-
tainable management of grassland ecosystem under
increasing N deposition, and points out that inter-
vention is needed to keep the N deposition rate of
the alpine meadow at a low rate, so as to increase
ANPP of the alpine meadow and provide
stable ecosystem functions and services for
humanity while maintaining the species richness
unchanged.
ACKNOWLEDGEMENTS
The authors thank Cheng Meng, Ying Shen and
Song Wang for their help in field measurement. We
thank the staff of Institute of Qinghai-Tibetan Pla-
teau in Southwest University for Nationalities. This
work was financially supported by the Strategic
Priority Research Program of the Chinese Academy
of Sciences (XDA23080302) and The Second Ti-
betan Plateau Scientific Expedition and Re-
search (STEP) program (2019QZKK0302), and
National Science Foundation of China (31625006).
DATA ACCESSIBILITY
Associated data are available in the supporting
information.
REFERENCES
Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJ. 2013. Trait-
based tests of coexistence mechanisms. Ecol Lett 16:1294–306.
Allan E, Weisser W, Weigelt A, Roscher C, Fischer M, Hillebrand
H. 2011. More diverse plant communities have higher func-
tioning over time due to turnover in complementary domi-
nant species. Proc National Acad Sci United States America
108:17034–9.
Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Han
X. 2010. Tradeoffs and thresholds in the effects of nitrogen
addition on biodiversity and ecosystem functioning: evidence
from inner Mongolia Grasslands. Global Change Biol 16:358–
72.
Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ,
Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug
ET, Armas C, Kikodze D, Cook BJ. 2002. Positive interactions
among alpine plants increase with stress. Nature 417:844–8.
Callaway RM, Walker LR. 1997. Competition and facilitation: a
synthetic approach to interactions in plant communities.
Ecology 78:1958–65.
Cardinale BJ, Gross K, Fritschie K, Flombaum P, Fox JW, Rixen
C, Ruijven JV, Reich PB, Scherer-Lorenzen M, Wilsey BJ.
2013. Biodiversity simultaneously enhances the production
and stability of community biomass, but the effects are inde-
pendent. Ecology 94:1697–707.
Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A,
Srivastava DS, Loreau M, Weis JJ. 2007. Impacts of plant
diversity on biomass production increase through time be-
cause of species complementarity. Proc National Acad Sci
104:18123–8.
Chen W, Zhang Y, Mai X, Shen Y. 2016. Multiple mechanisms
contributed to the reduced stability of Inner Mongolia grass-
land ecosystem following nitrogen enrichment. Plant and Soil
409:283–96.
Common Species Stability and Species Asynchrony Rather than Richness
Cottingham KL, Brown BL, Lennon JT. 2001. Biodiversity may
regulate the temporal variability of ecological systems. Ecol
Lett 4:72–85.
Dijkstra FA, Carrillo Y, Blumenthal DM, Mueller KE, LeCain DR,
Morgan JA, Zelikova TJ, Williams DG, Follett RF, Pendall E.
2018. Elevated CO
2
and water addition enhance nitrogen
turnover in grassland plants with implications for temporal
stability. Ecol Lett 21:674–82.
Doak DF, Bigger D, Harding EK, Marvier MA, O’Malley RE,
Thomson D. 1998. The statistical inevitability of stability-di-
versity relationships in community ecology. Am Naturalist
151:264–76.
Downing AL, Brown BL, Leibold MA. 2014. Multiple diversity–
stability mechanisms enhance population and community
stability in aquatic food webs. Ecology 95:173–84.
Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth
RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Hol-
land EA, Karl DM, Michaels AF, Porter JH, Townsend AR,
Smarty CJVR. 2004. Nitrogen cycles: past, present, and future.
Biogeochemistry 70:153–226.
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z,
Freney JR, Martinelli LA, Seitzinger SP, Sutton MA. 2008.
Transformation of the nitrogen cycle: Recent trends, ques-
tions, and potential solutions. Science 320.
Gomez-Casanovas N, Hudiburg TW, Bernacchi CJ, Parton WJ,
DeLucia EH. 2016. Nitrogen deposition and greenhouse gas
emissions from grasslands: uncertainties and future directions.
Global Change Biol 22:1348–60.
Gonzalez A, Loreau M. 2009. The causes and consequences of
compensatory dynamics in ecological communities. Ann Rev
Ecol Evol Syst 40:393–414.
Grime JP. 1998. Benefits of plant diversity to ecosystems:
immediate, filter and founder effects. J Ecol 86:902–10.
Grman E, Lau JA, Schoolmaster DR Jr, Gross KL. 2010. Mech-
anisms contributing to stability in ecosystem function depend
on the environmental context. Ecol Lett 13:1400–10.
Hautier Y, Seabloom EW, Borer ET, Adler PB, Harpole WS,
Hillebrand H, Lind EM, MacDougall AS, Stevens CJ, Bakker
JD, Buckley YM, Chu C, Collins SL, Daleo P, Damschen EI,
Davies KF, Fay PA, Firn J, Gruner DS, Jin VL, Klein JA, Knops
JM, La Pierre KJ, Li W, McCulley RL, Melbourne BA, Moore
JL, O’Halloran LR, Prober SM, Risch AC, Sankaran M, Schuetz
M, Hector A. 2014. Eutrophication weakens stabilizing effects
of diversity in natural grasslands. Nature 508:521–5.
Hautier Y, Tilman D, Isbell F, Seabloom EW, Borer ET, Reich PB.
2015. Anthropogenic environmental changes affect ecosystem
stability via biodiversity. Science 348:336–40.
Hector A, Hautier Y, Saner P, Wacker L, Bagchi R, Joshi J,
Scherer-Lorenzen M, Spehn EM, Bazeley-White E, Weilen-
mann M, Caldeira MC, Dimitrakopoulos PG, Finn JA, Huss-
Danell K, Jumpponen A, Mulder CPH, Palmborg C, Pereira JS,
Siamantziouras ASD, Terry AC, Troumbis AY, Schmid B,
Loreau M. 2010. General stabilizing effects of plant diversity
on grassland productivity through population asynchrony and
overyielding. Ecology 91:2213–20.
Hillebrand H, Bennett DM, Cadotte MW. 2008. Consequences of
dominance: a review of evenness effects on local and regional
ecosystem processes. Ecology 89:1510–20.
Humbert JY, Dwyer JM, Andrey A, Arlettaz R. 2016. Impacts of
nitrogen addition on plant biodiversity in mountain grasslands
depend on dose, application duration and climate: a system-
atic review. Global Change Biol 22:110–20.
Isbell F, Craven D, Connolly J, Loreau M, Schmid B,
Beierkuhnlein C, Bezemer TM, Bonin C, Bruelheide H, de
Luca E, Ebeling A, Griffin JN, Guo Q, Hautier Y, Hector A,
Jentsch A, Kreyling J, Lanta V, Manning P, Meyer ST, Mori
AS, Naeem S, Niklaus PA, Polley HW, Reich PB, Roscher C,
Seabloom EW, Smith MD, Thakur MP, Tilman D, Tracy BF,
van der Putten WH, van Ruijven J, Weigelt A, Weisser WW,
Wilsey B, Eisenhauer N. 2015. Biodiversity increases the
resistance of ecosystem productivity to climate extremes.
Nature 526:574–7.
Jiang L, Pu Z. 2009. Different effects of species diversity on
temporal stability in single-trophic and multitrophic commu-
nities. The American Naturalist 174:651–9.
Keitt TH. 2008. Coherent ecological dynamics induced by large-
scale disturbance. Nature 454:331–4.
Leps J. 2004. Variability in population and community biomass
in a grassland community affected by environmental pro-
ductivity and diversity. OIKOS 107:64–71.
Leps J, Majekova M, Vitova A, Dolezal J, Bello Fd. 2018. Sta-
bilizing effects in temporal fluctuations: management, traits,
and species richness in high-diversity communities. Ecology
99:360–71.
Li G, Sun S. 2011. Plant clipping may cause overestimation of
soil respiration in a Tibetan alpine meadow, southwest China.
Ecol Res 26:497–504.
Loreau M, de Mazancourt C. 2008. Species synchrony and its
drivers: neutral and nonneutral community dynamics in
fluctuating environments. Am Naturalist 172:E48–66.
Loreau M, de Mazancourt C. 2013. Biodiversity and ecosystem
stability: a synthesis of underlying mechanisms. Ecol Lett
16(Suppl 1):106–15.
Loreau M, Hector A. 2001. Partitioning selection and comple-
mentarity in biodiversity experiments. Nature 412:72–6.
Lu
¨C, Tian H. 2007. Spatial and temporal patterns of nitrogen
deposition in China: Synthesis of observational data. Journal
of Geophysical Research 112.
Ma F, Song B, Quan Q, Zhang F, Wang J, Zhou Q, Niu S. 2020.
Light competition and biodiversity loss cause saturation re-
sponse of net primary productivity to nitrogen enrichment.
Journal of Geophysical Research: Biogeosciences.
Ma F, Song B, Zhang F, Quan Q, Zhou Q, Niu S. 2018. Ecosys-
tem Carbon Use Efficiency Is Insensitive to Nitrogen Addition
in an Alpine Meadow. J Geophys Res Biogeosc 123:2388–98.
Ma Z, Liu H, Mi Z, Zhang Z, Wang Y, Xu W, Jiang L, He JS. 2017.
Climate warming reduces the temporal stability of plant
community biomass production. Nature Commun 8:15378.
Mulder CPH, Uliassi DD, Doak DF. 2001. Physical stress and
diversity-productivity relationships_ The role of positive
interactions. Proc National Acad Sci United States of America
98:6704–8.
Niu D, Yuan X, Cease AJ, Wen H, Zhang C, Fu H, Elser JJ. 2018.
The impact of nitrogen enrichment on grassland ecosystem
stability depends on nitrogen addition level. Sci Total Environ
618:1529–38.
Niu S, Wu M, Han YI, Xia J, Zhang ZHE, Yang H, Wan S. 2010.
Nitrogen effects on net ecosystem carbon exchange in a
temperate steppe. Global Change Biology 16:144–55.
Oliver TH, Isaac NJ, August TA, Woodcock BA, Roy DB, Bullock
JM. 2015. Declining resilience of ecosystem functions under
biodiversity loss. Nature Commun 6:10122.
Polley HW, Wilsey BJ, Derner JD. 2003. Do species evenness and
plant density influence the magnitude of selection and com-
F. Ma and others
plementarity effects in annual plant species mixtures. Ecol
Lett 6:248–56.
Romanuk TN, Vogt RJ, Kolasa J. 2006. Nutrient enrichment
weakens the stabilizing effect of species richness. OIKOS
114:291–302.
Sasaki T, Lauenroth WK. 2011. Dominant species, rather than
diversity, regulates temporal stability of plant communities.
Oecologia 166:761–8.
Sasaki T, Lu X, Hirota M, Bai Y, Allan E. 2019. Species asyn-
chrony and response diversity determine multifunctional
stability of natural grasslands. Journal of Ecology.
Song B, Sun J, Zhou Q, Zong N, Niu S. 2017. Initial shifts in
nitrogen impact on ecosystem carbon fluxes in an alpine
meadow: patterns and causes. Biogeosciences 14:3947–56.
Song L, Bao X, Liu X, Zhang F. 2012. Impact of nitrogen addition
on plant community in a semi-arid temperate steppe in China.
J Arid Land 4:3–10.
Steiner CF, Long ZT, Krumins JA, Morin PJ. 2005. Temporal
stability of aquatic food webs: partitioning the effects of spe-
cies diversity, species composition and enrichment. Ecol Lett
8:819–28.
Stevens CJ, Lind EM, Hautier Y, Harpole WS, Borer ET, Hobbie
S, Seabloom EW, Ladwig L, Bakker JD, Chu C, Collins S,
Davies KF, Firn J, Hillebrand H, Pierre KJL, Dougall AM,
Melbourne B, McCulley RL, Morgan J, Orrock JL, Prober SM,
Risch AC, Schuetz M, Wragg PD. 2015. Anthropogenic
nitrogen deposition predicts local grassland primary produc-
tion worldwide. Ecology 96:1459–65.
Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL,
Milchunas DG, Pennings S. 2005. Functional- and abun-
dance-based mechanisms explain diversity loss due to N fer-
tilization. Proc National Acad Sci United States of America
102:4387–92.
Tilman D. 1999. The ecological consequences of changes in
biodiversity: A search for general principles. Ecology 80:1455–
74.
Tilman D, Lehman CL, Bristow CE. 1998. Diversity-Stability
Relationships: statistical Inevitability or Ecological Conse-
quence? American Naturalist 151:277–82.
Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C.
2001. Diversity and productivity in a long-term grassland
experiment. Science 294:843–5.
Tilman D, Reich PB, Knops JM. 2006. Biodiversity and ecosys-
tem stability in a decade-long grassland experiment. Nature
441:629–32.
Valone TJ, Hoffman CD. 2003. Population stability is higher in
more diverse annual plant communities. Ecol Lett 6:90–5.
van Ruijven J, Berendse F. 2007. Contrasting effects of diversity
on the temporal stability of plant populations. OIKOS
116:1323–30.
Wayne Polley H, Wilsey BJ, Derner JD. 2007. Dominant species
constrain effects of species diversity on temporal variability in
biomass production of tallgrass prairie. OIKOS 116:2044–52.
Wilsey BJ, Daneshgar PP, Hofmockel K, Polley HW. 2014. In-
vaded grassland communities have altered stability-mainte-
nance mechanisms but equal stability compared to native
communities. Ecol Lett 17:92–100.
Wright AJ, Ebeling A, de Kroon H, Roscher C, Weigelt A,
Buchmann N, Buchmann T, Fischer C, Hacker N, Hildebrandt
A, Leimer S, Mommer L, Oelmann Y, Scheu S, Steinauer K,
Strecker T, Weisser W, Wilcke W, Eisenhauer N. 2015.
Flooding disturbances increase resource availability and pro-
ductivity but reduce stability in diverse plant communities.
Nature Commun 6:6092.
Wu Q, Ren H, Wang Z, Li Z, Liu Y, Wang Z, Li Y, Zhang R, Zhao
M, Chang SX, Han G, Hector A. 2020. Additive negative ef-
fects of decadal warming and nitrogen addition on grassland
community stability. Journal of Ecology.
Yang H, Jiang L, Li L, Li A, Wu M, Wan S. 2012. Diversity-
dependent stability under mowing and nutrient addition:
evidence from a 7-year grassland experiment. Ecol Lett
15:619–26.
Yang H, Li Y, Wu M, Zhang ZHE, Li L, Wan S. 2011a. Plant
community responses to nitrogen addition and increased
precipitation: the importance of water availability and species
traits. Global Change Biol 17:2936–44.
Yang H, Wu M, Liu W, Zhang ZHE, Zhang N, Wan S. 2011b.
Community structure and composition in response to climate
change in a temperate steppe. Global Change Biol 17:452–65.
Yang Z, Jiang L, Su F, Zhang Q, Xia J, Wan S. 2016. Nighttime
warming enhances drought resistance of plant communities in
a temperate steppe. Sci Rep 6:23267.
Yang Z, Jv R, Du G. 2011c. The effects of long-term fertilization
on the temporal stability of alpine meadow communities.
Plant Soil 345:315–24.
Yang Z, Zhang Q, Su F, Zhang C, Pu Z, Xia J, Wan S, Jiang L.
2017. Daytime warming lowers community temporal stability
by reducing the abundance of dominant, stable species. Global
Change Biol 23:154–63.
Zelikova TJ, Blumenthal DM, Williams DG, Souza L, LeCain DR,
Morgan J, Pendall E. 2014. Long-term exposure to elevated
CO
2
enhances plant community stability by suppressing
dominant plant species in a mixed-grass prairie. Proc National
Acad Sci United States America 111:15456–61.
Zhang Y, Feng J, Loreau M, He N, Han X, Jiang L. 2019. Nitrogen
addition does not reduce the role of spatial asynchrony in
stabilising grassland communities. Ecology Letters 22:563–71.
Zhang Y, Loreau M, He N, Zhang G, Han X. 2017. Mowing
exacerbates the loss of ecosystem stability under nitrogen
enrichment in a temperate grassland. Funct Ecol 31:1637–46.
Zhang Y, Loreau M, Lu X, He N, Zhang G, Han X. 2016. Nitrogen
enrichment weakens ecosystem stability through decreased
species asynchrony and population stability in a temperate
grassland. Global Change Biol 22:1445–55.
Zhang Y, Lu X, Isbell F, Stevens C, Han X, He N, Zhang G, Yu Q,
Huang J, Han X. 2014. Rapid plant species loss at high rates
and at low frequency of N addition in temperate steppe. Glob
Chang Biol 20:3520–9.
Zhao Y, Yang B, Li M, Xiao R, Rao K, Wang J, Zhang T, Guo J.
2019. Community composition, structure and productivity in
response to nitrogen and phosphorus additions in a temperate
meadow. Sci Total Environ 654:863–71.
Common Species Stability and Species Asynchrony Rather than Richness
A preview of this full-text is provided by Springer Nature.
Content available from Ecosystems
This content is subject to copyright. Terms and conditions apply.
