Journal of
Plant Ecology
Volume 7, Number 3,
Pages 231–239
June 2014
doi:10.1093/jpe/rtt030
Advance Access publication
6 July 2013
available online at
www.jpe.oxfordjournals.org
Linking flowering and reproductive
allocation in response to nitrogen
addition in an alpine meadow
Zhilong Zhang1,2, Kechang Niu3, Xudong Liu2, Peng Jia2
and Guozhen Du2,*
1
State Key Laboratory of Grassland Agroecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou
University, 768 West Jiayuguan Road, Lanzhou, Gansu 730020, People’s Republic of China
2
State Key Laboratory of Grassland Agroecosystems, School of Life Sciences, Lanzhou University, 222 Tianshui Road,
Lanzhou, Gansu 730000, People’s Republic of China
3
Department of Biology, Nanjing University, 22 Hankou Road, Nanjing, Jiangsu 210093, People’s Republic of China
*Correspondence address. State Key Laboratory of Grassland Agroecosystems, School of Life Sciences, Lanzhou
University, 222 Tianshui Road, Lanzhou, Gansu 730000, People’s Republic of China. Tel: +86-093-18912890;
Fax: +86-093-18912823; E-mail: [email protected]
Abstract
Aims
Plants can change in phenology and biomass allocation in response
to environmental change. It has been demonstrated that nitrogen is
the most limiting resource for plants in many terrestrial ecosystems.
Previous studies have usually focused on either flowering phenology
or biomass allocation of plants in response to nitrogen addition; however, attempts to link flowering phenology and biomass allocation
are still rare. In this study, we tested the effects of nitrogen addition on
both flowering phenology and reproductive allocation in 34 common
species. We also examined the potential linkage between flowering
time and reproductive allocation in response to nitrogen addition.
Methods
We conducted a 3-year nitrogen addition experiment in Tibetan
alpine meadow. We measured first flowering date and the reproductive allocation for 34 common plant species in control, low
and high nitrogen added plots, respectively. One-way analysis of
variance was used to examine differences of first flowering date
and reproductive allocation among treatments. The relationships
between the change in species first flowering date and change in
reproductive allocation in response to nitrogen addition were examined by calculating Pearson correlation coefficients.
Important Findings
For most species, both first flowering date and reproductive allocation significantly responded to nitrogen addition. Nitrogen addition
significantly delayed the first flowering date and reduced the reproductive allocation for all graminoid species, but accelerated flowering and increased reproductive allocation for most forb species. We
found that changes in first flowering date significantly negatively
correlated with the changes in reproductive allocation over species in response to nitrogen, which indicated a positive relationship
between flowering response and plant performance in reproductive
allocation. Species that advanced their flowering time with nitrogen
addition increased their reproductive allocation, whereas those that
delayed flowering time tended to decline in reproductive allocation with nitrogen addition. Our results suggest that species-specific
switch from vegetative growth to reproductive growth could influence species performance.
Keywords: alpine meadow, flowering, nitrogen addition,
reproductive allocation
Received: 23 December 2012, Revised: 15 May 2013, Accepted:
2 June 2013
Introduction
The response of plant phenological events to changes in
global climate has been a critical concern in ecology (Forrest
and Miller-Rushing 2010; Primack et al. 2004; Rathcke and
Lacey 1985, Visser and Both 2005). Recently, in the context
of rapid climate change, ecologists have gained renewed
interest in tracking plant phenology, such as the phenological
response to changes in temperature, precipitation, nutrient
availability and atmospheric concentration of carbon dioxide
(CO2) (Cleland et al. 2007; Fitter and Fitter 2002; Hovenden
et al. 2008; Huelber et al. 2006; Menzel 2003; Nord and Lynch
2009; Primack et al. 2004). Many studies found that nitrogen
addition could affect plant phenology (Baan 2006; Bowman
© The Author 2013. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
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232
et al. 2006; Cleland 2006; Diekmann and Falkengren-Grerup,
2002; Smith et al. 2012; Vitousek et al. 1997). For instance,
species showed different patterns in shifting of the phenology
due to evolution constraint (Kochmer and Handel 1986) or
life historical strategy (Diekmann and Falkengren-Grerup
2002; Kudo et al. 2008). Although theoretically it proposes
that the species-specific shifting of phenology plays important
roles in species performance, community structuring and
ecosystem functioning (Chuine and Beaubien 2001; Cleland
et al. 2007; Sherry et al. 2007; Forrest et al. 2010; Cleland et al.
2012), to our knowledge, the field tests are still lacking.
Flowering is a crucial developmental stage in the life cycle
for plants, which represents the phenological behaviour
by which plants begin allocating resources from their own
growth and survival to reproduction and offspring development (Roff 2002). A number of different factors, from
environmental to chemical, can trigger flowering. On the
population level, many studies have demonstrated that nitrogen addition could shift plant flowering (Baan 2006; Cleland
et al. 2006; Peñuelas et al. 1995; Smith et al. 2012), through
increasing plant growth rates and altering biomass allocation
(Marschner 1995). On the community level, the change in
flowering following nitrogen addition is more complex due
to combined effect of abiotic and biotic factors. Previous work
often focused on examining the shift of flowering time for
the dominant species, as these prevalent species could play
larger roles on ecosystem functioning (e.g. productivity) via
mass effect (Grime 1998) than non-dominant species. It is
well known that species diversity, including non-dominant
species, significantly influence community structure and ecosystem function via complementary effect (Cardinale et al.
2006). However, examination of the shift in flowering time
of all component species within a community in response to
nitrogen addition is needed.
The trade-off in biomass allocation results from physical
and chemical constraints during the life history of organisms
(Bazzaz and Grace 1997). One of the biological consequences
of flowering time shifting is relevant to species performance
(e.g. reproductive allocation). For example, nitrogen addition
inducing flowering time shifting may firstly lead to changes
on biomass allocation to reproductive structures. The asynchronous flowering time shifting among component species
should result asymmetrical change in reproductive allocation. Yet, on the community level, few studies have explored
the linkage between flowering time shifting and the change
in species reproductive allocation, which could help examine the effect of nitrogen addition on species performance as
well as community structure and ecosystem function. In this
study, we investigated the effect of nitrogen addition on the
flowering time and reproductive allocation for 34 common
species in an alpine meadow of the Qinghai-Tibet Plateau
for 3 years. Specifically, we asked the following three questions: (i) Whether nitrogen addition alters first flowering
date and reproductive allocation for these species? (ii) Do the
responses of first flowering date and reproductive allocation
to the nitrogen addition differ among component species? (iii)
Journal of Plant Ecology
Is the shift of flowering time correlated with the change in
reproductive allocation in response to nitrogen addition?
Materials and Methods
Study site
The experiment was conducted in an alpine meadow at The
Research Station of Alpine Meadow and Wetland Ecosystems
of Lanzhou University, in Maqu (N33°40′, E101°52′, altitude
3550 m), Gansu, China, on the eastern Tibetan Plateau. The
average temperature is 1.2°C, ranging from −10°C in January
to 11.7°C in July with ~270 frost days. The average yearly
precipitation, measured over the last 30 years, is 620 mm;
mainly occurring during the short and cool summer. The
annual cloud-free solar radiation is ~2580 h (Luo et al. 2006).
The vegetation is typical of alpine meadow on the Tibetan
Plateau, dominated by Kobresia graminifolia (Cyperaceae),
Elymus nutans (Poaceae), Anemone rivularis (Ranunculaceae),
Poa poophagorum (Poaceae), Festuca ovina (Poaceae) and Carex
kansuensis (Cyperaceae). The average above-ground biomass
is 360–560 g m-2 with 25–35 vascular plant species per 0.25
m2. The study site was fenced in 2008 with grazing by yak and
sheep only allowed during winter months.
Experimental design
In the late April 2009, twenty 10 m × 4 m blocks, separated
by 2–3 m, were established at the study site. In each block, we
established three 2 m × 4 m plots separated by 2 m. In each
plot, we randomly allocated control (CK, 0), low (LN, 5 g N m-2
year-1) and high (HN, 10 g N m-2 year-1) nitrogen addition treatments. For nitrogen addition treatment, a slow-release ammonium nitrate (NH4NO3) fertilizer was sprayed by hands once
annually at the beginning of May during drizzly days (Luo et al.
2006). Each plot was divided into two 2 m × 2 m subplots: one
for destructive sampling plant to measure reproductive allocation and the other for the phenology observation with a 0.5 m
× 0.5 m permanent quadrat located at its centre.
Measurements
Plant phenology was observed every 6–7 days from early
May to late September in each year. At each monitoring
time, plants with petals, anthers, filaments or calyx were
recognized as flowering. Flowering species were recorded
when the first flower appeared from any individual of focal
species present in the quadrats. The first flowering date was
recorded for each species in each quadrat as the number of
days after 1 January (Hovenden et al. 2008). Due to the loss of
some rare species following nitrogen addition (Luo et al. 2006;
Niu et al. 2008), we observed 8–20 replicates (quadrats) of
flowering time for 34 common species presented at all three
nitrogen addition treatments (see Appendix 1). These species
accounted for 90% (at CK) to 98% (at HN) of the communities
above-ground biomass. The 34 common species were also
chosen for measuring reproductive allocation. Samples
were collected when the focal species were flowering. Only
above-ground parts were collected due to the high density
Zhang et al. | Linking flowering and reproductive allocation in response to nitrogen addition233
of roots in the alpine community. We randomly chose 2–3
individuals for each species in the each 2 m × 2 m subplot,
resulting in total 20–30 individuals for each species for each
nitrogen addition treatment. For clonal species, a ramet was
regarded as an individual (Cheplick 1998; Luo et al. 2006).
Plants were dissected into vegetative parts (stems and leaves)
and reproductive parts (flowers). All samples were dried at
80°C for 48 h and weighed with a Sartorius balance (10–4 g
accuracy). Reproductive allocation was calculated as (biomass
of reproductive parts / total biomass) for each individual.
In each plot, we measured photosynthetically active radiation (PAR) at 10 cm above the soil surface and at the top of
the canopy with a Decagon Sunfleck ceptometer (Decagon,
Pullman, Washington, DC) on early August 2011 (most
graminoids are in flowering). PAR in understory was calculated by two level measurements (Li et al. 2011).
Statistical analysis
First, to analyze the effect of nitrogen addition on the first
flowering date and reproductive allocation for each species, we
used the one-way analysis of variance (ANOVA) to examine
differences of first flowering date and reproductive allocation
among different nitrogen addition treatments, and the
significance differences between treatments were identified
using the least significant difference test. One-way ANOVA
was also used to analyze the effect of nitrogen addition on
PAR in the understorey. Then, we calculated the response of
first flowering date to low nitrogen addition treatment and
high nitrogen addition treatment as the value of FFDLN −
FFDCK and FFDHN − FFDCK, respectively, where FFDLN, FFDHN
and FFDCK were the mean first flowering date of a species in
low nitrogen addition, high nitrogen addition and controlled
plots, respectively. Thus, a positive or negative value indicates
that nitrogen addition treatments delayed or accelerated first
flowering date, respectively. We calculated the change in
species reproductive allocation response to low nitrogen and
high nitrogen treatments as the value of ln (RALN/RACK) and
ln (RAHN/RACK), where RALN, RAHN and RACK are the mean
reproductive allocation of a species in low nitrogen, high
nitrogen and controlled plots, respectively (Niu et al. 2008).
A positive or negative value indicates that nitrogen addition
treatments increased or decreased reproductive allocation,
respectively. Finally, we examined the relationships between
the changes in species first flowering date and reproductive
allocation in response to nitrogen addition by calculating
Pearson correlations. All statistical analysis was done using
SPSS 16.0. For the analysis presented here, we focus on the
data of 2011 growing season—the third year of the experiment.
Results
Effect of nitrogen addition on species first
flowering date and reproduction allocation
Nitrogen addition significantly altered first flowering date for
most species. The effect of nitrogen addition on first flowering date differed between graminoids and forbs. Compared
with control, both low nitrogen and high nitrogen treatment significantly delayed the first flowering date for almost
graminoid species (P < 0.05; Fig. 1A and B). Compared with
control, the first flowering date was significantly accelerated for most forb species in low and/or high nitrogen treatment (P < 0.05), but significantly delayed for two forb species
(Saussurea hieracioides and S. nigrescens) in the high nitrogen
treatment (P < 0.05; Fig. 1). Additionally, first flowering date
did not respond significantly to nitrogen addition for two legume species (Fig. 1A and B).
The response of reproductive allocation to nitrogen addition varied among species. All of graminoid species trends to
reduce reproductive allocation in response to both low nitrogen and high nitrogen treatment. This response was statistically significant for five of the eight graminoid species in the
low nitrogen treatment and for all eight graminoid species in
the high nitrogen treatment (P < 0.05; Fig. 2A and B). For
forb species, reproductive allocation decreased in some species but increased in other species in the response to nitrogen
addition. Three and six forb species significantly decreased
reproductive allocation in response to low and high nitrogen addition, respectively (P < 0.05; Fig. 2A and B). Four and
eight forb species significantly increased reproductive allocation in low and high nitrogen addition, respectively (P < 0.05;
Fig. 2A and B). Some forb species did not significantly change
reproductive allocation following nitrogen addition.
Relationship between change in species flowering
time and reproduction allocation
We found the changes of first flowering date were significantly negatively correlated with the changes of reproductive
allocation in response to nitrogen addition (in low nitrogen
added plots: r = −0.616, P < 0.001; in high nitrogen added
plots: r = −0.626, p < 0.001; Fig. 3). Biologically, this indicates
species that accelerated flowering time with nitrogen addition increased their reproductive allocation, whereas those
that delayed flowering time decreased reproductive allocation
with nitrogen addition. In that sense, the real relationship
between the response of flowering time and species reproductive allocation is actually positive.
Comparing with control, the PAR (68%) in understorey
(>10 cm near the soil surface) was significantly decreased in
both low (18%, P < 0.05) and high nitrogen addition treatment (11%, P < 0.05).
Discussion
Species-specific response of first flowering date and
reproduction allocation
The timing of reproductive events indicates a trade-off
between vegetative and reproductive growth (Bolmgren and
Cowan 2008; Elzinga et al. 2007). Our results showed that, for
most species, both first flowering date and reproductive allocation significantly responded to nitrogen addition. Species
are different either in the response direction or in the change
of the first flowering date and reproductive allocation.
234
Journal of Plant Ecology
Figure 1: the response of 34 alpine common species’ first flowering date (FFD) to low nitrogen addition (LN, A) and high nitrogen addition
treatment (HN, B). The asterisks (*) indicate the significant differences between control and nitrogen addition treatments (P < 0.05).
Generally, consistent with previous studies (Cleland et al.
2006; Niu et al. 2008), we found graminoid species tend to
delay flowering and decrease reproductive allocation, whereas
most forb species tend to accelerate flowering and increase
reproductive allocation in response to nitrogen addition. The
delay of flowering indicates that plants delayed the switch
from vegetative growth to reproduction, which may result
from increased vegetative growth and/or clone reproduction
(Cleland et al. 2006). In contrast, accelerated flowering and
the increase of reproductive allocation suggest plants tend to
increase productive growth in response to nitrogen addition.
As addressed in our previous studies, the size-dependent
response of biomass allocation is associated with the enhanced
competition (Niu et al. 2008, 2009). In nitrogen added plots,
size-dependent asymmetric competition for light and soil
resource is a main driver of community assembly (Rajaniemi
et al. 2003, Schwinning and Weiner 1998). Graminoid species
with higher leaf allocation and clone growth often have larger
individuals that confer them in a competitive advantage
of competitive exclusion (Niu et al. 2008, 2009) and/or
assemblage-level self-thinning (Luo et al. 2006; Stevens and
Carson 1999). Additionally, graminoid species tend to acquire
and use nitrogen to increase biomass more rapidly than that of
neighbouring forbs (Bowman et al. 2006). In line with previous
results, in this study, we found graminoid species increased
competitive ability not only by increasing vegetative allocation
but also by delaying flowering time. By increasing vegetative
growth, graminoid species became more competitive for limiting
light, used the added nitrogen (Gleeson and Tilman 1990;
Leishman 2001; Tilman 1988) and became more abundant or
even dominated in nitrogen added plots (Ashton et al. 2010;
Suding et al. 2005; Zavaleta et al. 2003). In contrast, accelerated
flowering and increased reproductive allocation in most forb
species suggest that forb species take a different response
strategy in nitrogen added plots (Cleland et al. 2006). Niu et al.
(2009) addressed that the change in reproductive allocation of
forbs not only resulted from the change in individual size but
also partly from size-independent change of trade-offs between
vegetative growth and reproduction. By accelerated flowering
and increased reproductive allocation, forb species may change
trade-offs towards reproduction in expense of competitive
ability in response to enhanced competition in nitrogen added
plots. Theoretically, this advantage makes forb species produce
more seeds and increase colonization to meta-communities.
However, we found that the allocation to seeds decreased
following fertilization (Niu et al. 2008, 2009). It is possible
that enhanced pollination limitation in nitrogen added plots
results in this incongruent pattern. Therefore, further studies
Zhang et al. | Linking flowering and reproductive allocation in response to nitrogen addition235
Figure 2: the response of 34 alpine common species’ reproductive allocation (RA) to low nitrogen addition (LN, A) and high nitrogen addition
treatment (HN, B). The asterisks (*) indicate the significant differences between control and nitrogen addition treatments (P < 0.05).
scaling up plant performance to species fitness and biodiversity
assembly are needed. Noteworthy, we found two forb species
(S. hieracioides and S. nigrescens) significantly delayed flowering
and decreased reproductive allocation in response to nitrogen
addition. The delayed flowering of other forb species were
also reported in other nitrogen addition studies from alpine
regions (Baan 2006; Smith et al. 2012). Unlike most forb species
flowering in early and mid-growing season, both species belong
to late flowering species. This suggests that, beyond species
functional group, other attributes may be also very important
influencing the response strategy of flowering. To clarify why
species are different either in response direction or magnitude
of the change, more functional comprehensive experiment and
comparative analysis should be applied in the further studies.
Linking flowering time and reproductive
allocation in response to nitrogen addition
Theoretically, the shift in flowering time inevitably causes
change in biomass allocation, which influences plant performance (as discussed above) and species fitness as well as
community structuring and ecosystem functioning. Through
meta-analysis, Cleland et al. (2012) found that the advanced
phenology of species with warming also increased species
performance, whereas those without advanced phenology tended to decline in performance with warming. To our
knowledge, there have been no such studies directly linking
the species-specific response of phenology to the change in
plant performance following nitrogen addition. Fortunately,
some attempts have inferred consequences of the phenology
change on species performance (Cleland et al. 2012) or ecosystem function (Cleland et al. 2006, 2007).
Our results demonstrated that the species (most forb species)
with accelerated flowering often tended to increase reproductive
allocation, whereas species (graminoid species) that delayed
flowering often decreased reproductive allocation. This leads
to a significantly positive relationship between flowering
response and species performance in reproductive allocation.
For most species, we found significant changes in reproductive
allocation among treatments. Basically, the changes stem from
direct and indirect effects of nitrogen addition on reproductive
allocation. Although it is hard to directly discriminate these
two effects in this study, we infer that the relative importance
of the direct and indirect effects could differ between forbs
and graminoid species. For most forb species, the change in
reproductive allocation mainly stems from the direct effect
of nitrogen addition on reproductive allocation—individual
236
Figure 3: the relationship between first flowering date (FFD) and
reproductive allocation (RA) in response to low (LN) and high (HN)
nitrogen addition treatments. Each symbol indicates the difference of
mean value of first flowering date and reproductive allocation in LN
(square and dash line) or HN (triangle and solid line) from control.
size rapidly increased at early growing season accompanying
increased accumulation of reproductive biomass in relatively
extended flowering period at mid-growing and later growing
season. For graminoid species, the change in reproductive
allocation mainly results from indirect effect mediated by
competition—continued increase of vegetative growth to
compete for limited light caused a delay in flowering, which
resulted in further decreases in biomass accumulation in the
shortened flowering period. Taking advantage of early seedling
emergence (mostly in late April and early May), added soil
nutrition and more water available (thawing of frozen ground
in April and more rainfall in May and June), most forb species
rapidly increased size to flowering at early and mid-growing
season before most graminoid species grow up to flowering.
After flowering, these forb species mainly allocated fixed
resource (e.g. biomass) to reproductive growth in mid-growing
and later growing season, which resulted increase in biomass
of reproductive structure larger than increase of individual
size and we observed increased reproductive allocation. When
using flowering time as a covariant in analysis of covariance
analysis (data not show), we found that reproductive
allocation still significantly differed among treatments for most
forb species. This supported our above inference that change
in reproductive allocation mainly resulted from direct effect
of nitrogen addition. In contrast, seedlings of most graminoid
species emerged relatively late and were often surrounded
by large forbs early in the growing season (May and early
Journal of Plant Ecology
June). Hence, graminoid species continued to increase in size
(e.g. allocating more fixed biomass to leaves) to compete for
limiting light before flowering. This indicates that enhanced
competition caused remarkable increase of individual size
and the delay of flowering in graminoid species. At Tibetan
alpine meadow with very short growth season, this delay
in flowering by 5–6.5 days further significantly influences
the accumulation of reproductive biomass. When we used
flowering time as a covariant to examine the change of
reproductive allocation in response to nitrogen addition, we
did not find significant differences among treatments for
graminoid species on reproductive allocation. This further
supports our argument that the decrease of reproductive
allocation mainly resulted from delayed flowering time
rather than direct effect of nitrogen addition. As similar
with graminoid species, delayed flowering and decreased
reproductive allocation in two forb species (S. hieracioides
and S. nigrescens) with later seedling emergence also suggest
that the response of flowering and reproductive allocation
is tightly related with seedling emergence and competition.
Theoretically, the decrease of reproductive allocation will
result in seed limitation in nitrogen added plots further. Due
to the fact that most graminoid species have clonal growth,
they could be abundant at local plots in a short term. However,
their colonization ability to meta-communities may decline
with the multiple-year nitrogen addition. Additionally, it is
interesting that two legumes did not significantly change in
flowering time and reproductive allocation following nitrogen
addition, which was also reported in another study (Cleland
et al. 2006). We propose that the legume, with early seedling
emergence and nitrogen fixing capacity, may not significantly
respond to soil nitrogen addition.
In short, both direct and indirect effects of nitrogen addition
results in the change in reproductive allocation. Flowering,
considered as a key life history event, will significantly influence reproductive allocation, but its relative importance in scenario of nitrogen addition still needs to be clarified. By directly
linking flowering and reproductive allocation in response to
nitrogen addition, our study supports Cleland et al. (2012),
who recently proposed that advanced phenology with climate change will increase species performance, whereas species without advanced phenology will decline in performance.
Apparently, enhanced competition is the main driver of community assembly and key interaction among species following
nitrogen addition. Competition will significantly influence both
first flowering date and reproductive allocation, but other factor, such as facilitation and pollination may also play important
roles in determining flowering and reproductive allocation. The
linkage between phenology and species performance needs
more exploration with comprehensive and long-term studies.
Funding
National Natural Science Foundation of China (40930533,
41171214).
Zhang et al. | Linking flowering and reproductive allocation in response to nitrogen addition237
Acknowledgements
We thank Dr Chengjin Chu and Dr Tarek W. Elnaccash for supporting in English writing revision and valuable suggestion on the article.
We thank Gefei Zhang, Zhikuo Li, Honglin Li, Wei Li, Wenxiang Hu,
Weixin Zhu, Wen Liu, Xuexue Qin, Xin Yin for their valuable help
during the experiments. We also thank Jane G. Smith for her helpful
comments on the original article.
Appendix 1
First flower date (FFD) of 34 species in response to three different nitrogen addition treatments in an alpine meadow of the QinghaiTibet Plateau during the 2011 growing season. CK, LN and HN indicate treatments of nitrogen addition control: (CK: 0 g N m-2
year-1), low nitrogen addition treatment: (LN: 5 g N m-2 year-1) and high nitrogen addition treatment: (HN: 10 g N m-2 year-1).
‘Number’ indicates the plot numbers with where flowers present at all the three nitrogen addition treatments. Dates are reported
as mean Julian day ± SE, where n = 8–20. Different small letters in the same row indicate a significant difference (P < 0.05)
between treatments.
Species
CK
LN
HN
Number
205 ± 1.41a
13
207 ± 2.35
207 ± 1.3a
15
Graminoids
Agrostis gigantea
200 ± 1.18b
203 ± 0.73a
b
a
Agrostis trinii
202 ± 1.65
Elymus nutans
198 ± 1.14b
203 ± 1.37a
206 ± 2.01a
10
Festuca ovina
200 ± 1.53b
203 ± 3.16ab
206 ± 2.57a
14
Kobresia capillifolia
134 ± 1.96b
139 ± 2.57a
142 ± 2.8a
20
Poa poophagorum
194 ± 1.57b
198 ± 1.48a
199 ± 1.58a
16
a
b
ab
Poa pratensis
198 ± 2.19
204 ± 1.03
207 ± 3.61
14
Roegneria nutans
202 ± 1.65b
206 ± 2.24a
209 ± 2.35a
15
228 ± 2.57a
224 ± 2.46b
222 ± 3.48b
10
150 ± 1.49
146 ± 1.73b
17
Forbs
Allium sikkimense
a
ab
Anemone obtusiloba
151 ± 1.95
Anemone rivularis
183 ± 1.29a
182 ± 1.95a
179 ± 2.11a
16
Anemone trullifolia
152 ± 1.37a
148 ± 1.69b
146 ± 2.57b
16
Aster diplostephioides
199 ± 2.69a
201 ± 1.82a
201 ± 2.27a
10
Astragalus polycladus
184 ± 4.48
a
185 ± 3.44
a
187 ± 3.19
a
11
Delphinium kamaonense
225 ± 4.91a
219 ± 1.6a
219 ± 1.48a
10
Euphorbia esula
150 ± 1.96a
146 ± 1.47b
143 ± 1.37b
17
Euphrasia regelii
199 ± 3.33a
200 ± 4.15a
202 ± 4.95a
11
Galium verum
195 ± 1.38a
191 ± 2.21b
189 ± 1.26b
10
Gentiana aristata
205 ± 2.56a
203 ± 2.76ab
199 ± 3.11b
10
Gentiana sino-ornata
253 ± 2.75a
250 ± 2.6b
246 ± 1.41b
10
Halenia elliptica
208 ± 1.07a
204 ± 2.6b
200 ± 2.63b
11
Leontopodium nanum
191 ± 2.88a
191 ± 0a
194 ± 2.67a
11
a
a
a
Ligularia virgaurea
196 ± 5.9
198 ± 1.6
200 ± 2.67
8
Oxytropis ochrocephala
206 ± 3.92a
207 ± 1.79a
206 ± 1.47a
12
Parnassia trinervis
202 ± 3a
203 ± 2.25a
203 ± 1.8a
9
189 ± 1.04
187 ± 2.45b
9
185 ± 2.3a
184 ± 2.42a
183 ± 1.93a
16
Ranunculus tanguticus
187 ± 1.43a
186 ± 1.51a
184 ± 2.39a
15
Rumex patientia
180 ± 4.88a
176 ± 3b
174 ± 1.2b
9
Saussurea hieracioides
202 ± 3b
204 ± 3.37ab
206 ± 3a
Pedicularis kansuensis
193 ± 4.05
Potentilla fragarioides
a
b
ab
ab
9
a
Saussurea nigrescens
208 ± 2.78
210 ± 0.9
213 ± 2.29
10
Thalictrum alpinum
150 ± 1.43a
145 ± 1.51b
143 ± 0.67b
12
Tongoloa tenuifolia
206 ± 4.41a
203 ± 4.5ab
200 ± 4.02b
11
Veronica eriogyne
195 ± 2.51a
192 ± 2.59ab
190 ± 3.05b
12
238
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