Ecological Applications, 25(3), 2015, pp. 848–855
Ó 2015 by the Ecological Society of America
Species-abundance–seed-size patterns within a plant community
affected by grazing disturbance
GAO-LIN WU,1,2,3 ZHAN-HUAN SHANG,2,4,5 YUAN-JUN ZHU,1,3 LU-MING DING,2,4
AND
DONG WANG1,3
1
2
State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation,
Northwest A&F University, Yangling, Shaanxi 712100 China
State Key Laboratory of Grassland Agro-Ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University,
Lanzhou 730020 China
3
Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resources, Yangling,
Shaanxi 712100 China
4
School of Life Sciences, Lanzhou University, Lanzhou 730000 China
Abstract. Seed size has been advanced as a key factor that inﬂuences the dynamics of
plant communities, but there are few empirical or theoretical predictions of how community
dynamics progress based on seed size patterns. Information on the abundance of adults,
seedlings, soil seed banks, seed rains, and the seed mass of 96 species was collected in alpine
meadows of the Qinghai-Tibetan Plateau (China), which had different levels of grazing
disturbance. The relationships between seed-mass–abundance patterns for adults, seedlings,
the soil seed bank, and seed rain in the plant community were evaluated using regression
models. Results showed that grazing levels affected the relationship between seed size and
abundance properties of adult species, seedlings, and the soil seed bank, suggesting that there
is a shift in seed-size–species-abundance relationships as a response to the grazing gradient.
Grazing had no effect on the pattern of seed-size–seed-rain-abundance at four grazing levels.
Grazing also had little effect on the pattern of seed-size–species-abundance and pattern of
seed-size–soil-seed-bank-abundance in meadows with no grazing, light grazing, and moderate
grazing), but there was a signiﬁcant negative effect in meadows with heavy grazing. Grazing
had little effect on the pattern of seed-size–seedling-abundance with no grazing, but had
signiﬁcant negative effects with light, moderate, and heavy grazing, and the jr j values
increased with grazing levels. This indicated that increasing grazing pressure enhanced the
advantage of smaller-seeded species in terms of the abundances of adult species, seedlings, and
soil seed banks, whereas only the light grazing level promoted the seed rain abundance of
larger-seeded species in the plant communities. This study suggests that grazing disturbances
are favorable for increasing the species abundance for smaller-seeded species but not for the
larger-seeded species in an alpine meadow community. Hence, there is a clear advantage of the
smaller-seeded species over the larger-seeded species with increases in the grazing level.
Key words: abundance; grazing gradient; seed bank; seed rain; seed mass; seedlings.
INTRODUCTION
An understanding of vegetation dynamics is basic to
the manipulation of plant communities (Niering 1987,
Rees et al. 2001). Ecologists have long sought to
understand how so many species can coexist in the same
community (Shipley et al. 2006, Laughlin et al. 2012).
Community maintenance and dynamics were a focal
point in the last few decades for ecological research,
which was mainly concerned with the determinants of
plant life histories, species composition, diversity,
productivity, and stability (Grubb 1977, Tilman 1988,
Coomes and Grubb 2003). The neutral theory assumes
that all individuals of all species are functionally
equivalent, i.e., individuals do not have species-speciﬁc
Manuscript received 22 January 2014; revised 20 August
2014; accepted 29 August 2014; ﬁnal version received 19
September 2014. Corresponding Editor (ad hoc): Y. Zhang.
5 Corresponding author. E-mail: [email protected]
848
traits inﬂuencing their ﬁtness, longevity, movements or
likelihood of speciation, and thus this theory predicts
that any given species trait should be uncorrelated with
its abundance in a community (Hubbell 2001). Recent
research on biodiversity and ecosystem functions gave a
new impetus to understanding community ecological
processes that focused on the effects of current
environmental changes on species, in terms of species
distributions and patterns of species diversity (Loreau
2010). Ecologists sought general explanations for the
dramatic variation in species abundances in space and
time (Adler et al. 2014). An increasingly popular
solution was to predict species distributions, dynamics,
and responses to environmental change based on plant
functional traits (McGill et al. 2006, Shipley et al. 2006,
Cornwell and Ackerly 2009, Laughlin et al. 2012),
especially seed size (Moles et al. 2007, Adler et al. 2014).
Uriarte and Reeve (2003) combined considerations of
ecological and evolutionary dynamics to investigate trait
April 2015
SPECIES-ABUNDANCE–SEED-SIZE PATTERNS
evolution and community assembly, with particular
focus on the seed size of species within communities. A
classic problem was addressed: the diversity of seed sizes
among coexisting plant species. Differences in seed size
among species are related to differences in seed
production and seedling establishment and growth, with
seed size underlying a trade-off between these traits
(Muller-Landau 2003). Some models were also expected
to predict correlation between seed size and abundance
in natural communities. One possible explanation is that
the affected processes (e.g., seed production and seedling
performance in the case of seed size) are particularly
important for ﬁtness (Coomes and Grubb 2003),
because seed size is a better phenomenological indicator
of a strategy coordinated across functions and life stages
(Adler et al. 2014). There is a positive correlation
between seed mass and abundance in the absence of seed
sowing (Levine and Rees 2002, Turnbull et al. 2005).
Many studies have reported that seed size has
important evolutionary and ecological meaning within
and among species. Seed size is a key factor inﬂuencing
the dynamics of interspeciﬁc interactions and the
mechanisms of coexistence in a plant community (Rees
and Westoby 1997, Rees et al. 2001, Coomes and Grubb
2003, Muller-Landau 2003, Adler et al. 2014). This is
because seed size can signiﬁcantly affect seed dispersal,
seed germination, seedling emergence, survival, and
plant morphologies, life histories, and physiologies
(Rees et al. 2001, Coomes and Grubb 2003, Wu et al.
2013), which are strongly correlated with plant abundances in many communities (Guo 2003, Muller-Landau
2003, Murray and Leishman 2003, Eriksson 2005,
Fenner and Thompson 2005). Larger seeds are assumed
to have a higher probability of successful recruitment
than smaller seeds. This is because larger seeds give rise
to larger seedlings and larger seedlings better withstand
environmental hazards such as deep shade and drought.
The advantage of larger seeds in recruitment success is
pronounced in deeply shaded habitats (Bruun and Brink
2008). Seed size is discussed as an integrative topic when
studying species diversity coexistence in plant communities, since different species with seed size can adjust
their population growth rates to adapt to different
resource availability and interspeciﬁc competition
(Coomes and Grubb 2003, Muller-Landau 2003). Leishman and Murray (2001) suggested that communities are
dominated by the smaller-seeded species, which have
good dispersal capacities in the early successional stages,
but are dominated by the larger-seeded species, which
have competitive superiority, in the later successional
stages (Coomes et al. 2002).
Therefore, seed size patterns should have great
relevance to developing an understanding of vegetation
dynamics and coexistence, and the functioning of the
plant community. Additionally, disturbance has been
deﬁned as an important mechanism that facilitates the
maintenance of species diversity in the plant community
(Connell 1978, Kadmon and Benjamini 2006). Distur-
849
bances in the form of different grazing levels have been
shown to result in different offspring recruitment in
alpine meadow communities (Wu et al. 2011). However,
to our knowledge, no previous study has empirically
evaluated the relative importance of seed size patterns in
plant community structure along a grazing gradient. In
this study, we sought to use the current understanding of
seed size variation to explain patterns in plant relative
abundance along a grazing gradient. To understand the
effects of the grazing level on seed size-abundance
patterns and community dynamics, we examined the
relationships between the seed size and species abundances of four life-history stages (adult, seedling, seed
rain, and soil seed bank). The main objectives of the
study were (1) to determine empirically the seed-size–
species-abundance pattern in the community components of adults, seedlings, soil seed bank, and seed rain;
(2) to explore whether grazing levels affected the seedsize–species-abundance pattern in a community; and (3)
to study the responses of the seed-size–species-abundance pattern under different grazing levels in an alpine
meadow community.
MATERIALS
AND
METHODS
Study site
A series of experiments and investigations were
carried out in alpine meadows (Dawu, Qinghai Province; 33843 0 to 35816 0 N, 98848 0 to 100855 0 E) at a mean
altitude of over 4000 m on the Qinghai-Tibetan Plateau,
China. In the studied area, the climate is cold with long
harsh winters and short cool summers. The annual mean
precipitation is 542.1 mm, with most rainfall (445.0 mm)
falling between May and September. The annual mean
air temperature is 2.38C. The duration of sunshine in
the growing season is 2450.8 h. The vegetation typiﬁes
alpine meadows, which consist mainly of arctic-alpine
and Chinese Himalayan plants and are dominated by
Kobresia tibetica swamp meadow, Stipa aliena meadow,
Kobresia pygmaea meadow, and Kobresia capillifolia
meadow. There are 20–30 vascular plant species per
quadrat (0.25 m2).
Experiment design and data collection
To evaluate the relationships between seed mass and
species abundance of aboveground vegetation, seedlings, seed rain, and seed bank along a grazing gradient,
four plots were set up in an alpine meadow, each plot
having a different grazing level: UN, undisturbed with
no grazing; LG, light grazing; MG, moderate grazing;
and HG, heavy grazing (Table 1). The four studied
plots had all undergone the same level of nomadic
grazing by Tibetan sheep and yaks belonging to local
herders in the last few decades. From 1995 onward,
grazing tenure was implemented in this area and, as part
of this process, some grasslands were fenced off with
grazing exclusion under the government project ‘‘Returning to Grassland by Eliminating Grazing.’’ The
undisturbed meadow plots with no grazing were set up
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Vol. 25, No. 3
GAO-LIN WU ET AL.
TABLE 1. Description of the vegetation and basic study site properties including the soil properties of the 0–20 cm soil layer for the
study alpine meadow plots.
Mean stocking
rates (head/hm2)
Vegetation
cover (%)
Grazing levels
Latitude and longitude
Altitude (m)
Undisturbed meadow with no
grazing (UN)
Light grazing (LG)
34831.673 0 N; 100802.064 0 E
3972
0
80–95
34828.921 0 N; 100813.067 0 E
3732
0.77
60–75
Moderate grazing (MG)
34828.748 0 N; 100813.159 0 E
3728
1.29
40–60
3745
1.81
50–75
Heavy grazing (HG)
0
0
34827.856 N; 100812.524 E
Notes: ‘‘Head’’ refers to the number of stock animals. Values are mean 6 SE.
in these fenced meadows. The other three grazing-level
plots were set up on the sheep ranches of different
families. They were all situated in freely grazed
meadows but the grazing levels could be clearly deﬁned
by the known stocking rates based on the number of
sheep per unit area (head/hm2). Furthermore, the
herders had maintained these stocking rates at a
relatively stable level, with free grazing, during the 10
years prior to this study, and they were also maintained
throughout the study. Grazing levels were determined
based on the stocking rates according to the method of
Wu et al. (2009). The stocking rates of the meadows
with light grazing, moderate grazing, and heavy grazing
were 0.77, 1.29, and 1.81 head/hm2, respectively. Mean
stocking rates, vegetation cover, and dominant species,
and the soil water content, soil pH value, soil organic
matter, and total nitrogen contents of the 0–20 cm soil
layer in each meadow are given in Table 1.
All the four plots were keep current grazing situations
about 10 years. The grazing levels were keeping during
our investigation periods. We calculated the stocking
rates of four grazing disturbance gradients. Stocking
rates were calculated by identiﬁed grassland area and the
number of sheep units (head/hm2). The unperturbed
meadow with no grazing disturbance was fenced to
exclude livestock grazing for 10 years. The stocking rates
of the light-disturbance meadow, the medium-disturbance meadow, and the heavy-disturbance meadow were
0.77, 1.29, and 1.81 head/hm2, respectively. In this
study, 15 ﬁxed sampling quadrats (i.e., ﬁve quadrats [50
3 50 cm] in each of the three sampling plots [30 3 50 m],
one per grazing level) were established for community
investigations (adults and seedlings). An additional 15
sampling quadrats were set up, adjacent to the ﬁrst 15
quadrats, thus creating 15 pairs of quadrats in all, for
sampling the soil seed bank. All of the quadrats had the
same orientation, and the same slope aspect and
position. The sample citing was carried out according
to the classiﬁcation of grasslands in the study region
(Ma et al. 2002, Dong et al. 2005, Shang 2006).
The whole study was conducted from April 2006 to
December 2007. Community investigations were based
on the same 15 ﬁxed sampling quadrats (50 3 50 cm)
throughout the study period. The new recruitment
seedling numbers of each species were investigated
monthly from June to August using the methods
described by Welling and Laine (2000), and preceded
the adult individuals investigation. The numbers of
adult individuals (for clonal adult species, a ramet was
regarded as an individual) were measured for each
species in each quadrat during the peak of the growing
season in August 2006.
The soil seed banks were sampled using the remaining
15 ﬁxed quadrats. Sampling was carried out at the
beginning of March 2006, which was before seed
germination began in order to assess the persistent
portions of the seed banks. In each quadrat, 10 cores (5
cm diameter) from 0–15 cm depths were sampled at
regular intervals across the quadrat (Baskin and Baskin
1998). Seedling germination was assessed after ﬁrst
concentrating the samples by removing most of the soil
(ter Heerdt et al. 1996) and keeping them in a
refrigerator (temperature 48C) for 4 months. All the
seed bank samples were refrigerated (temperature 48C)
for 4 months. Seedling germination was then assessed
after ﬁrst concentrating the samples by removing most
of the soil (ter Heerdt et al. 1996). The seedling
germination investigation was conducted under conditions of the naturally ﬂuctuating temperature of the
surface soil with constant water content according to
local ﬁeld conditions, which began in May 2007 and
ended in September 2007. Five months after beginning
the germination investigation, the remaining soil was
removed by washing with water over a ﬁne sieve and the
remaining ungerminated seeds were counted. For each
species, the mean sum of the number of germinated
seedlings and the number of the residual seeds was its
seed bank number in the soil.
Seed rain collection was based on the methods of
Booth and Larson (1998) for samples collected at ﬁxed
locations within the plots from May 2007 until
November 2007. In each sampling plot, 30 seed-catch
implements (10 3 6 3 2 cm) were set up in an equidistant
(1 m) arrangement (Aerts et al. 2006).
Information about diversity and aboveground individuals, seedlings, seed rain, and the soil seed bank of
each species were collected. The mean species abundance, seedling numbers, seed rain numbers, and soil
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SPECIES-ABUNDANCE–SEED-SIZE PATTERNS
851
TABLE 1. Extended.
Soil water
content (%)
pH
Soil organic
matter content (%)
Total soil nitrogen
content (%)
71.35 6 0.95
6.46 6 0.01
9.63 6 0.17
0.89 6 0.04
33.14 6 0.55
7.69 6 0.01
4.16 6 0.12
0.55 6 0.02
30.00 6 0.25
7.79 6 0.02
3.45 6 0.17
0.45 6 0.02
28.66 6 0.50
7.98 6 0.02
2.85 6 0.05
0.38 6 0.02
Dominant species
Kobresia humilis, Kobresia capillifolia,
Kobresia pygmaea
Poa crymophila, Elymus nutans, Kobresia
pygmaea
Oxytropis ochrocephala, Heteropappus
altaicus, Kobresia humilis
Aconitum pendulum, Lagotis
brachystachya, Carum carvi
seed bank numbers of each species in a given plot were
calculated.
A total of 96 species, occurring as 61 adult species, 56
seedling species, 56 soil seed bank species, and 48 seed
rain species, were found in the surveys. Seeds of each
species were collected from nearby sites when mature
between the years 2006 and 2007. Seeds were air dried
and kept in the laboratory. To estimate seed mass, seeds
from the collections were pooled, eight samples consisting of 100 seeds for each species were weighed, and then
the mean seed mass per seed for a species was calculated.
evaluated using linear regression. The differences in seed
abundance data along the grazing gradients (or among
grazing levels) were analyzed using ANCOVA, with the
grazing levels as ﬁxed factors and seed size as a
covariate. Seed mass and abundance data were in all
cases log10 -transformed prior to these analyses. Statistical, regression, and ANOVA analyses, followed by a
post hoc test to identify signiﬁcant differences among
the means of each factor at each grazing level, were
carried out using SPSS 13.0 (SPSS, Chicago, Illinois,
USA) software.
Statistical analyses
RESULTS
To avoid confusion, the species density, seedlings
density, seed rain density, and soil seed bank density
(numbers of individuals per sampling quadrat) were
used as surrogates for the mean species abundance per
square meter, mean number of seedlings per square
meter, mean number of seeds in seed rain per square
meter, and mean number of seeds in soil seed bank per
square meter for each species as described by Guo (2003)
and by Murray and Leishman (2003). The relationships
between seed mass and either species density, seedling
density, seed rain density, or soil seed bank density were
Species abundance and seed rain abundance did differ
signiﬁcantly either among grazing levels or seed sizes
according to the ANCOVA (Table 2). However, seed
size had signiﬁcant effects on seedling abundance (F3,56
¼ 7.437; P , 0.01) and on soil seed bank abundance
(F3,56 ¼ 8.965; P , 0.01), but grazing levels did not
signiﬁcantly affect them (Table 2). Table 3 presents
detailed information about the linear regressions.
Neither the relationship between seed mass and species
abundance nor that between seed mass and soil seed
bank abundance were signiﬁcant at grazing levels of no
TABLE 2. The statistical signiﬁcance of the effects of grazing levels on the abundances of plant
community components determined by ANCOVA with seed size as the covariate.
Source
df
Type I
sum of squares
Aboveground species abundance
Grazing levels
Seed size
Error
3
1
105
Seedling abundance
Grazing levels
Seed size
Error
Soil seed bank abundance
Grazing levels
Seed size
Error
Seed rain abundance
Grazing levels
Seed size
Error
Note: All data were log-transformed.
F
P
0.581
0.809
74.930
0.271
1.134
0.846
0.289
3
1
106
1.200
2.935
41.830
1.013
7.437
0.390
0.007
3
1
108
1.243
3.420
41.202
1.086
8.965
0.358
0.003
3
1
69
2.107
0.195
29.172
1.662
0.461
0.183
0.499
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GAO-LIN WU ET AL.
grazing, light grazing, and moderate grazing, but both
relationships were signiﬁcant, exhibiting a negative
correlation, at the heavy grazing level. Seedling abundance followed a different pattern in that its relationship
with seed mass was not signiﬁcant at the no-grazing
level, but was signiﬁcant, exhibiting negative correlations, at levels of light grazing, moderate grazing, and
heavy grazing; furthermore, the absolute determination
coefﬁcient jr j values increased with increasing levels of
grazing. No signiﬁcant relationship between seed mass
and seed rain abundance at any grazing level was found
(Table 3), which indicated that grazing had no effect on
the pattern of seed-size–seed-rain-abundance in this
study.
The grazing level had signiﬁcant effects on seed-mass–
species-abundance patterns among the alpine meadow
community components of adults, seedlings, the soil
seed bank, and seed rain. Maximum species diversity
occurred in aboveground vegetation and seed rain in the
undisturbed meadow with no grazing, and in seedlings
and in the soil seed bank under light grazing (Table 3).
With the increases in grazing pressure, the smallerseeded species had higher adult individual abundance,
seedling recruitment abundance and soil seed bank
abundance than the larger-seeded species. However, in
the undisturbed meadow with no grazing, the opposite
results were obtained (Fig. 1a–c). Seed rain in the light
grazing meadow exhibited larger-seeded species with
higher abundance, while in the other three meadows
with no grazing, moderate grazing, and heavy grazing
levels, it was the smaller-seeded species that had the
higher abundance (Fig. 1d).
DISCUSSION
Our results suggested that grazing level affected the
relationships between seed size and abundance properties of adult species, seedlings, and the soil seed bank,
and that there was a shift in seed-size–species-abundance
relationships as a response to the grazing levels in the
studied alpine meadow communities. In the present
study, we found that grazing level could alter the
relationship between seed size and dominance for
coexistent species within communities, which was
consistent with the ﬁndings of a previous study (Wu et
al. 2009). In the undisturbed meadow, seed size was
positively related to both adult and seedling abundances. This result supported the concept that larger-seeded
species would generally outcompete the smaller-seeded
species (Lonnberg and Eriksson 2012, 2013), as well as
game theoretical models applied to maintenance of seed
size diversity in general, irrespective of whether the
mechanism behind the seed size effect was competition
or stress tolerance (Rees and Westoby 1997). This
coexistence of multiple seed size strategies is usually
explained by a mechanism driven by a tradeoff between
stress tolerance and fecundity (Muller-Landau 2010).
Another important result that we found was that all
of the relationships between seed size and the plant
community properties of the abundances of adult
species, seedlings, and the soil seed bank at all grazing
levels were negative except for that between seed size
and seed rain abundance at the light grazing level. The
larger-seeded species that were usually considered to
exhibit greater germination rates and seedling survival,
were found to have higher survival rates, accelerated
germination timing, enhanced seedling growth, and
larger individual biomass (Leishman and Westoby
1994, Westoby et al. 1997, Leishman et al. 2000,
Burmeier et al. 2010, Wu et al. 2013). Lonnberg and
Eriksson (2013) found that the larger seeds generally had
an advantage over the smaller seeds in direct contests for
perennial herbs growing under shade conditions in
southeastern Sweden. There was also a positive effect
of seed size on seedling recruitment (Lonnberg and
Eriksson 2012). However, the larger-seeded species were
also subject to weaker dispersal and lower probability of
escape from predation (Go`mez 2004) since the larger
seeds and individuals with greater biomass were more
convenient food sources for herbivores in grassland.
Our results indicated that light grazing levels increased seed rain abundance of the larger-seeded species.
This can be explained by the light grazing level
facilitating the loosing of seeds and dispersal availability
of seed rains in the plant community, which was in
accordance with the intermediate disturbance hypothesis
that there exists a hump-shaped pattern between
community diversity and disturbance (Connell 1978,
Catford et al. 2012). However, there was an increased
TABLE 3. Linear regression correlations between seed mass
and plant community components for different grazing
levels.
Grazing levels
n
r
P
Aboveground species abundance
UN
LG
MG
HG
35
24
30
24
0.077
0.171
0.103
0.437
0.330
0.424
0.588
0.033
Seedling abundance
UN
LG
MG
HG
27
33
25
29
0.264
0.355
0.426
0.470
0.183
0.043
0.034
0.010
Soil seed bank abundance
UN
LG
MG
HG
28
34
25
29
0.106
0.201
0.376
0.483
0.590
0.254
0.064
0.008
Seed rain abundance
UN
LG
MG
HG
25
15
14
23
0.213
0.283
0.161
0.174
0.306
0.307
0.583
0.428
Notes: n refers to the total number of species used in the
analyses; P is the probability; and r is the determination. P
values ,0.05 are shown in boldface type. Grazing levels are
UN, undisturbed with no grazing; LG, light grazing; MG,
moderate grazing; and HF, heavy grazing.
April 2015
SPECIES-ABUNDANCE–SEED-SIZE PATTERNS
853
FIG. 1. Relationships between seed size (mg) and (a) species density (number of individuals of a species/m2), (b) seedling density
(number of seedlings/m2), (c) soil seed bank density (number of seeds in seed bank/m2), and (d) seed rain density (number of seeds
in seed rain/m2) for different grazing levels in an alpine meadow: UN, undisturbed, no grazing; LG, light grazing; MG, moderate
grazing; and HG, heavy grazing. Correlation coefﬁcients are given in Table 3.
probability that seeds would be eaten by animals at the
higher grazing levels, especially the larger-seeded species.
Conversely, the smaller-seeded species had a stronger,
holistic, adaptive life-history strategy to grazing that
gave them an advantage over the larger-seeded species in
the alpine meadow community (Coomes and Grubb
2003, Fenner and Thompson 2005). The smaller-seeded
species produced larger numbers of seeds (Smith and
Fretwell 1974), especially when competing under conditions of reduced resources where the larger-seeded
species tended to be eaten. The ﬁtness of the smallerseeded species estimated by these components was
signiﬁcantly lower than the ﬁtness of the larger-seeded
species under grazing conditions.
Our results also suggested that the grazing level had a
signiﬁcant effect on the external and potential dynamics
of community succession and made important contributions to observed seed-size–abundance patterns for
adult, seedlings, the soil seed bank, and seed rain in the
plant community. With increasing grazing intensity, the
advantages of species density, biomass, and frequency
were switched from the larger-seeded species to the
smaller-seeded species within the community, which was
consistent with the ﬁndings of a previous study (Wu et
al. 2009). Grazing level signiﬁcantly changed the species
coexistence patterns based on seed size in the plant
community. From the aspect of vegetation succession,
the previous study of Wu et al. (2009) had predicted that
communities in early successional stages were dominated by the smaller-seeded species with good dispersal
capacities (Leishman and Murray 2001, Coomes et al.
2002, Mouquet et al. 2004, Wu et al. 2011). As
succession progressed, communities were dominated by
the larger-seeded species with competitive superiority
(Leishman and Murray 2001, Murray and Leishman
2003, Murray et al. 2005), which was consistent with our
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Vol. 25, No. 3
GAO-LIN WU ET AL.
results under the no grazing condition. The increased
grazing pressure enhanced the advantage of the smallerseeded species for adults and seedlings and for soil seed
bank abundances in plant communities. This also
suggested that the smaller-seeded species had a stronger,
holistic, adaptive life-history strategy to grazing disturbance that gave them an advantage over the largerseeded species in the alpine meadow community as
mentioned above. Meanwhile, biotic and abiotic limitations to seedling growth and survival, and conversely
availability of safe sites for recruitment, varied along
environmental gradients and among habitat types
(Bruun and Brink 2008). All of these results indicated
that the smaller-seeded species tended to become more
dominant throughout the community (i.e., in terms of
adult, seedling, seed bank, and seed rain densities) than
the larger-seeded species with increasing grazing pressure.
In general, grazing disturbances were more favorable
to species abundance increases for the smaller-seeded
species than for the larger-seeded species in the alpine
meadow community. This indicated that there was a
clear advantage of the smaller-seeded species over the
larger-seeded species with increasing levels of grazing.
This study revealed the external (adult and seedlings
abundances) and potential (soil seed bank and seed rain
abundances) dynamics of community succession. The
succession would undergo a change from a community
dominated by the larger-seeded species to a community
dominated by the smaller-seeded species with increasing
levels of grazing.
CONCLUSION
The patterns of seed-size–species-abundance found in
this study may contribute to a more general understanding of grazing effects on alpine grassland ecosystems, as well as to better-founded approaches in plant
diversity conservation and grassland grazing management. Our results show that grazing levels affect the
relationships between seed size and abundance properties of adult species, seedlings and the soil seed bank,
and that there is a shift in seed-size–species-abundance
relationships in response to grazing gradients. These
suggest that increasing the grazing pressure enhances the
competitive advantage of the smaller-seeded species for
the abundances of adult species, seedlings, and the soil
seed bank, but that only the light grazing level promoted
the seed rain abundance of the larger-seeded species in
the plant communities. In general, grazing disturbances
favor species abundance increases for the smaller-seeded
species than for the larger-seeded species in the alpine
meadow community. This indicates that there was a
clear advantage of the smaller-seeded species over the
larger-seeded species with increasing levels of grazing.
ACKNOWLEDGMENTS
This research was funded by the Projects of Natural Science
Foundation of China (NSFC41371282, 30900177, 41171417),
the Strategic Priority Research Program—Climate Change:
Carbon Budget and Related Issues of the Chinese Academy of
Sciences (CAS) (Grant No. XDA05050403), the Project of
Natural Science Foundation of Shaanxi Province (2014KJXX15), and Program for New Century Excellent Talents in
University (NCET-13-0261). We are grateful to two anonymous reviewers for helpful feedback on earlier versions of the
manuscript.
LITERATURE CITED
Adler, P. B., R. Salguero-Go´mez, A. Compagnoni, J. S. Hsu, J.
Ray-Mukherjee, C. Mbeau-Ache, and M. Franco. 2014.
Functional traits explain variation in plant life history
strategies. Proceedings of the National Academy of Sciences
USA 111:740–745.
Aerts, R., W. Maes, E. November, M. Behailu, J. Poesen, J.
Deckers, M. Hermy, and B. Muys. 2006. Surface runoff and
seed trapping efﬁciency of shrubs in a regenerating semiarid
woodland in northern Ethiopia. Catena 65:61–70.
Baskin, C. C., and J. M. Baskin. 1998. Seeds, ecology,
biogeography and evolution of dormancy and germination.
Academic Press, San Diego, California, USA.
Booth, B. D., and D. W. Larson. 1998. The role of seed rain in
determining the assembly of a cliff community. Journal of
Vegetation Science 9:657–668.
Bruun, H. H., and D. J. T. Brink. 2008. Recruitment advantage
of large seeds is greater in shaded habitats. Ecoscience
15:498–507.
Burmeier, S., T. W. Donath, A. Otte, and R. L. Eckstein. 2010.
Rapid burial has differential effects on germination and
emergence of small-and large-seeded herbaceous plant
species. Seed Science Research 20:189–200.
Catford, J. A., C. C. Daehler, H. T. Murphy, A. W. Sheppard,
B. D. Hardesty, D. A. Westcott, M. Rejma´nek, P. J.
Bellingham, J. Pergl, and C. C. Horvitz. 2012. The
intermediate disturbance hypothesis and plant invasions:
implications for species richness and management. Perspectives in Plant Ecology, Evolution and Systematics 14:231–
241.
Connell, J. H. 1978. Diversity in tropical rain forest and coral
reefs. Science 199:1302–1310.
Coomes, D. A., and P. J. Grubb. 2003. Colonization, tolerance,
competition and seed-size variation within functional groups.
Trends in Ecology and Evolution 18:283–291.
Coomes, D. A., M. Rees, P. J. Grubb, and L. Turnbull. 2002.
Are differences in seed mass among species important in
structuring plant communities? Evidence from analyses of
spatial and temporal variation in dune-annual populations.
Oikos 96:421–432.
Cornwell, W. K., and D. D. Ackerly. 2009. Community
assembly and shifts in plant trait distributions across an
environmental gradient in coastal California. Ecological
Monographs 79:109–126.
Dong, Q. M., X. Q. Zhao, Y. S. Ma, Q. Y. Li, Q. J. Wang, and
J. J. Shi. 2005. Regressive analysis between stocking rate for
yak and aboveground and underground biomass of warmseason pasture in Kobrecia parva alpine meadow. [In Chinese
with English abstract.] Pratacultural Science 22:65–71.
Eriksson, O. 2005. Game theory provides no explanation for
seed size variation in grasslands. Oecologia 144:98–105.
Fenner, M., and K. Thompson. 2005. The ecology of seeds.
Cambridge University Press, Cambridge, UK.
Go`mez, J. M. 2004. Bigger is not always better: Conﬂicting
selective pressures on seed size in Quercus ilex. Evolution
58:71–80.
Grubb, P. J. 1977. The maintenance of species-richness in plant
communities: the importance of regeneration niche. Biological Reviews 52:107–145.
Guo, Q. F. 2003. Plant abundance: the measurement and
relationship with seed size. Oikos 101:639–642.
April 2015
SPECIES-ABUNDANCE–SEED-SIZE PATTERNS
Hubbell, S. 2001. The uniﬁed neutral theory of biodiversity and
biogeography. Princeton University Press, Princeton, New
Jersey, USA.
Kadmon, R., and Y. Benjamini. 2006. Effects of productivity
and disturbance on species richness: a neutral model.
American Naturalist 167:939–946.
Laughlin, D. C., C. Joshi, P. M. van Bodegom, Z. A. Bastow,
and P. Z. Fule´. 2012. A predictive model of community
assembly that incorporates intraspeciﬁc trait variation.
Ecology Letters 15:1291–1299.
Leishman, M. R., and B. R. Murray. 2001. The relationship
between seed size and abundance in plant communities:
model predictions and observed patterns. Oikos 94:151–161.
Leishman, M. R., and M. Westoby. 1994. The role of large
seeds in seedling establishment in dry soil conditions—
experimental evidence for semi-arid species. Journal of
Ecology 82:249–258.
Leishman, M. R., I. J. Wright, A. T. Moles, and M. Westoby.
2000. The evolutionary ecology of seed size. Pages 31–57 in
M. Fenner, editor. Seeds: the ecology of regeneration in plant
communities. Second edition. CABI International, Wallingford, Oxford, UK.
Levine, J. M., and M. Rees. 2002. Coexistence and relative
abundance in annual plant assemblages: the roles of
competition and colonization. American Naturalist
160:452–467.
Lonnberg, K., and O. Eriksson. 2012. Seed size and recruitment
patterns in a gradient from grassland to forest. Ecoscience
19:140–147.
Lonnberg, K., and O. Eriksson. 2013. Rules of the seed size
game: contests between large-seeded and small-seeded
species. Oikos 122:1080–1084.
Loreau, M. 2010. Linking biodiversity and ecosystems: towards
a unifying ecological theory. Philosophical Transactions of
the Royal Society B 365:49–60.
Ma, Y. S., B. N. Lang, Q. Y. Li, J. J. Shi, and Q. M. Dong.
2002. Study on rehabilitating and rebuilding technologies for
degenerated alpine meadow in the Changjiang and Yellow
River source region. [In Chinese with English abstract.]
Pratacultural Science 19:1–4.
McGill, B. J., B. J. Enquist, E. Weiher, and M. Westoby. 2006.
Rebuilding community ecology from functional traits.
Trends in Ecology and Evolution 21:178–185.
Moles, A. T., D. D. Ackerly, J. C. Tweddle, J. B. Dickie, R.
Smith, M. R. Leishman, M. M. Mayﬁeld, A. Pitman, J. T.
Wood, and M. Westoby. 2007. Global patterns in seed size.
Global Ecology and Biogeography 16:109–116.
Mouquet, N., P. Leadley, J. Me’riguet, and M. Loreau. 2004.
Immigration and local competition in herbaceous plant
communities: a three-year seed sowing experiment. Oikos
104:77–90.
Muller-Landau, H. C. 2003. Seeds of understanding of plant
diversity-traits important to competitive ability are variable
and subject to evolutionary change. Proceedings of the
National Academy of Sciences USA 100:1469–1471.
Muller-Landau, H. C. 2010. The tolerance–fecundity tradeoff
and the maintenance of diversity in seed size. Proceedings of
the National Academy of Sciences USA 107:4242–4247.
Murray, B. R., B. P. Kelaher, G. C. Hose, W. F. Figueira, and
M. R. Leishman. 2005. A meta-analysis of the interspeciﬁc
855
relationship between seed size and plant abundance within
local communities. Oikos 110:191–194.
Murray, B. R., and M. R. Leishman. 2003. On the relationship
between seed mass and species abundance in plant communities. Oikos 101:643–645.
Niering, W. A. 1987. Vegetation dynamics (succession and
climax) in relation to plant community management.
Conservation Biology 1:287–295.
Rees, M., R. Condit, M. Crawley, S. Pacala, and D. Tilman.
2001. Long-term studies of vegetation dynamics. Science
293:650–655.
Rees, M., and M. Westoby. 1997. Game-theoretical evolution
of seed mass in multi-species ecological models. Oikos
78:116–126.
Shang, Z. H. 2006. Studies on soil seed bank and regeneration
of degraded alpine grassland in the headwaters of Yangtze
and Yellow Rivers on Tibetan Plateau. Dissertation. Gansu
Agricultural University, Lanzhou, China.
Shipley, B., D. Vile, and E. Garnier. 2006. From plant traits to
plant communities: a statistical mechanistic approach to
biodiversity. Science 314:812–814.
Smith, C. C., and D. Fretwell. 1974. The optimal balance
between size and number of offspring. American Naturalist
108:499–506.
ter Heerdt, G. N. J., G. L. Verweij, R. M. Berker, and J. P.
Bakker. 1996. An improved method for seed bank analysis:
seedling emergence after removing the soil by sieving.
Functional Ecology 10:144–151.
Tilman, D. 1988. Plant strategies and the dynamics and
structure of plant communities. Princeton University Press,
Princeton, New Jersey, USA.
Turnbull, L. A., L. Manley, and M. Rees. 2005. Niches, rather
than neutrality, structure a grassland pioneer guild. Proceedings of the Royal Society B 272:1357–1364.
Uriarte, M., and H. K. Reeve. 2003. Matchmaking and species
marriage: a game-theory model of community assembly.
Proceedings of the National Academy of Sciences USA
100:1787–1792.
Welling, P., and K. Laine. 2000. Characteristics of the seedling
ﬂora in alpine vegetation, subarctic Finland, I. Seedling
densities in 15 plant communities. Annals Botanici Fennici
37:69–76.
Westoby, M., M. Leishman, and J. Lord. 1997. Comparative
ecology of seed size and dispersal. Pages 143–162 in J.
Silvertown, M. Franco, and J. L. Harper, editors. Plant life
histories, ecology, phylogeny and evolution. Cambridge
University Press, Cambridge. UK.
Wu, G. L., G. Z. Du, and Z. H. Shi. 2013. Germination
strategies of twenty alpine species with varying seed mass and
light availability. Australian Journal of Botany 61:404–411.
Wu, G. L., W. Li, X. P. Li, and Z. H. Shi. 2011. Grazing as a
mediator of offspring diversity maintenance: sexual and
clonal recruitment in grassland communities. Flora—Morphology, Distribution, Functional Ecology of Plants
206:241–245.
Wu, G. L., X. P. Li, J. M. Cheng, X. H. Wei, and L. Sun. 2009.
Grazing disturbances mediate species composition of alpine
meadow based on seed size. Israel Journal of Ecology and
Evolution 55:369–379.