Stoichiometry of Root and Leaf Nitrogen and Phosphorus in a Dry Alpine Steppe on the Northern Tibetan Plateau
Wu J (2014) Stoichiometry of Root and Leaf Nitrogen and Phosphorus in a Dry Alpine Steppe on the Northern Tibetan Plateau. PLoS
ONE 9(10): e109052. doi:10.1371/journal.pone.0109052
Stoichiometry of Root and Leaf Nitrogen and Phosphorus in a Dry Alpine Steppe on the Northern Tibetan Plateau
Jiangtao Hong 0
Xiaodan Wang 0
Jianbo Wu 0
Liping Zhu, Institute of Tibetan Plateau Research, China
0 1 Institute of Mountain Hazards and Environment, Chinese Academy of Sciences , Chengdu , China , 2 University of Chinese Academy of Sciences , Beijing , China
Leaf nitrogen (N) and phosphorus (P) have been used widely in the ecological stoichiometry to understand nutrient limitation in plant. However,few studies have focused on the relationship between root nutrients and environmental factors. The main objective of this study was to clarify the pattern of root and leaf N and P concentrations and the relationships between plant nitrogen (N) and phosphorus (P) concentrations with climatic factors under low temperature conditions in the northern Tibetan Plateau of China. We conducted a systematic census of N and P concentrations, and the N:P ratio in leaf and root for 139 plant samples, from 14 species and 7 families in a dry Stipa purpurea alpine steppe on the northern Tibetan Plateau of China. The results showed that the mean root N and P concentrations and the N:P ratios across all species were 13.05 mg g21, 0.60 mg g21 and 23.40, respectively. The mean leaf N and P concentrations and the N:P ratio were 23.20 mg g21, 1.38 mg g21, and 17.87, respectively. Compared to global plant nutrients concentrations, plants distributing in high altitude area have higher N concentrations and N:P, but lower P concentrations, which could be used to explain normally-observed low growth rate of plant in the cold region. Plant N concentrations were unrelated to the mean annual temperature (MAT). The root and leaf P concentrations were negatively correlated with the MAT, but the N:P ratios were positively correlated with the MAT. It is highly possible this region is not N limited, it is P limited, thus the temperaturebiogeochemical hypothesis (TBH) can not be used to explain the relationship between plant N concentrations and MAT in alpine steppe. The results were valuable to understand the bio-geographic patterns of root and leaf nutrients traits and modeling ecosystem nutrient cycling in cold and dry environments.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its
Supporting Information files.
Funding: This study was supported by the Western Action Plan Project of the Chinese Academy of Sciences (Grant No. KZCX2-XB3-08), the Strategic Pilot Science
and Technology Projects of the Chinese Academy of Sciences (Grant No. XDB03030505). The funders had no role in study design, data collection and analysis,
decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
Nitrogen (N) and phosphorus (P) are two essential elements in
plants, both playing a critical role in plant function and most
ecosystem processes . A number of studies have reported
species-specific differences (growth form, physiology, life history,
etc.) and site-specific differences (temperature, precipitation, solar
radiation, etc.) that account for much of the variability in
plantnutrient concentrations on large scales .
Temperature could be an important factor that drive the
recirculation of nutrients in terrestrial ecosystems. Lower
temperatures have depressing effect on microbial decomposition and
mineralization of organic matter, which drastically reduce nutrient
availability for plant [7,8]. Furthermore, low-temperature
supressing of nutrient uptake by root and soil nutrients migration are also
well known phenomena . Thus, Reich and Oleksyn 
assumed that the global leaf N concentrations generally increased
with the mean annual temperature (MAT) when the temperature
was below 510uC (the temperature-biogeochemical hypothesis).
Shi et al.  found the similar variation trend that leaf N
concentrations increased with MAT under low temperature (MAT
, 8.5uC) along an altitudinal gradient of Mount Gongga on the
eastern Tibetan Plateau. However, other study reported that
temperature had no effects on leaf concentrations, but
phylogenetic variation was the key factor that affected the leaf N
concentrations at the biome scale . Wheather the
temperaturebiogeochemical hypothesis (TBH) could be used to explain the
relationship between leaf N concentrations and MAT in alpine
area is still a controversial issue on account of few plant data
contained in previous studies [3,4,9]. In addition, the underlying
mechanism of temperature on regulating leaf N in cold
environment also deserves a further discussion.
Although ecological stoichiometry has been studied in terrestrial
plants for many years, and most of studies focused on
photosynthetic organs , we know little about the characteristics of
root-nutrient stoichiometry along the climate gradient at a large
scale, especially in cold and dry areas . For example, Yuan
et al.  compiled fine-root nitrogen and phosphorus data from
211 studies in 51 countries and reported that fine-root N:P
declined exponentially, but leaf N:P decreased linearly with the
increasing latitude (decreasing temperature) at global scale.
However, only 11 species were compiled from tundra ecosystem
in their study. The paucity of data limited not only the accurate
evaluation of elements involved in biogeochemical cycles but also
our understanding of plant nutrient concentrations response to the
environmental factors under low temperature. Therefore, we need
to provide a valuable contribution to the global data pool on root
stoichiometry, given the previously limited knowledge on the
We studied the spatial patterns of leaf and root nutrients from
139 plant samples and their relationship with climatic variables at
32 sites distributed from east to west across the northern Tibetan
Plateau. Our objectives were (1) to clarify the pattern of root and
leaf N and P concentrations; (2) to quantify the relationship
between plant nutrition and climatic factors, including MAT and
mean annual precipitation (MAP) in a cold and dry climate.
Materials and Methods
The Tibetan Plateau, the highest plateau in the world, is
extremely sensitive to climate change, and the vegetation has
remained largely undisturbed by human activities; therefore, it is
an important area to study global change ecology . The
alpine steppe in the northern Tibetan Plateau is a dry Stipa
purpurea grassland with low precipitation, frequent gale-force
winds, strong solar radiation and extensive permafrost. These
have a profound effect on the soil nutrient status, the evolution of
physiological processes and the adaptive mechanisms of plants
[17,18]. The study area was Stipa purpurea alpine steppe, located
between 31.23uN32.31uN and 80.12uE91.35uE. The study sites
were in seven counties (Nakchu, Palgon, Shantsa, Nima, Gerts,
Gakyi and Gar) from east to west in the Tibet Autonomous
Region of China with the similar soil type . The sites were
selected on flat terrain far from human habitats to minimise the
influence of microtopography and grazing disturbance. Most sites
were above 4500 m, with MAT below 0uC and MAP below
300 mm (Fig. 1; Table S1). The geographic information, such as
latitude, longitude and altitude, of each site was recorded by a
Global Positioning System (GPS) (Garmin, GPSMAP 62S,
We selected 32 sites along a belt transect (approx. 1300 km
long) and collected 139 plant samples from 14 species and 7
CV 0.37 0.29
Figure 2. The relationship between the N and P concentrations (b) and the N:P ratio (a, c) for roots and leaves across all species on
the northern Tibetan Plateau. The solid line represents the root fitted straight line, the dashed line represents the leaf fitted straight line.
families in August 2012 (Appendix). Each sample (15 cm length,
15 cm width, 30 cm depth) included the dominant species that
was abundant at each site, and these samples were dug up using a
spade. Then impurities on leaf and root surface were carefully
cleaned. Individuals from the same species were combined,
sundried in a paper envelope and brought back to the laboratory. In
each sampling site, no specific permissions were required for
collecting samples and the field studies did not involve endangered
or protected species.
Plants were divided into roots and leaves, oven-dried at 65uC to
a constant weight and ground into fine powder with a
plantsample grinder (TAISITE, High-speed Universal Disintegrator
FW80, Tian Jin, China). The total N concentration was
determined using the micro-Kjeldahl method after digesting the
sub-samples in H2SO4-K2SO4-CuSO4 . For the total P
concentration determination, the sub-samples were digested in a
H2SO4-HClO4 solution, and the P concentration was determined
using phosphor molybdate blue spectrophotometry . All the
data were expressed as a mass (mg g21).
The climate data from 1950 to 2000 for the sampling sites,
including MAT and MAP, were obtained from the World Climate
web site (www.worldclimate.com) with a resolution of 300 (ca.
1 km) .
The data of root and leaf N,P and N:P ratio exhibited
nonnormal distribution in the present study. Therefore, the N and P
concentrations and the N:P ratios were log-transformed to meet
normality for Pearson correlation and regression analysis and
TTests, as is commonly done in analyses of plant N:P stoichiometry
[6,911].The differences in the leaf N and P concentrations and
N:P ratios between the northern Tibetan Plateau and the other
region were processed using independent sample T-Tests. The
correlations of root and leaf N and P concentrations and N:P ratios
were analysed with regression analysis. The effects of the MAT
and MAP on root and leaf N and P concentrations and N:P ratios
were tested by Pearson correlation analysis and simple regression
analyses. All of the statistical analyses were performed with SPSS
version 16.0 (SPSS Inc., USA), and cartograms were plotted using
OriginPro 8.0 (OriginLab, MA).
Patterns of N and P concentrations and the N:P ratio in
roots and leaves across all species
The mean values of root N and P concentrations and the N:P
ratio were 13.05 mg g21, 0.60 mg g21 and 23.40 (Table 1). The
average values of leaf N and P concentrations and the N:P ratio
were 23.20 mg g21, 1.38 mg g21 and 17.87, respectively (Table 1).
The root and leaf N and P concentrations were positively correlated
with each other (root: R2 = 0.13, P,0.001; leaf: R2 = 0.40, P,
0.001, see Fig. 2b). The root and leaf N:P ratios were more strongly
correlated with P concentrations (root: R2 = 0.36, P,0.001; leaf:
R2 = 0.37, P,0.001) than with N concentrations (root: R2 = 0.26,
P,0.001; leaf: R2 = 0.05, P,0.01, see Fig. 2a, c).
Root N and P concentrations and N:P ratio were positively
correlated with leaf N and P concentrations and N:P ratio,
respectively. (N: R2 = 0.52, P,0.001; P: R2 = 0.34, P,0.001; N:P:
R2 = 0.21, P,0.001, see Fig. 3a, b, c).
Relationship of N and P concentrations and the N:P ratio
in roots and leaves with climate factors
Across all species, both the root and leaf N concentrations were
not significantly correlated with the MAT and MAP (P.0.05),
while the root and leaf P concentrations were negatively
correlated with the MAT [root: correlation coefficient (r) = 2
0.26, P,0.01; leaf: r = 20.20, P,0.05] (Table 2). Positive linear
correlations were detected between the N:P ratio and the MAT
for roots and leaves (root: r = 0.19, P,0.05; leaf: r = 0.30, P,
0.001). However, the root and leaf N:P ratio had no significant
relationship with the MAP (P.0.05). In addition, the leaf P
concentration was negatively correlated with the MAP (r = 2
0.17, P,0.05) but not with the root P concentration (P.0.05)
(Table 2, Fig. 4, Fig. 5).
Patterns of root and leaf N and P concentrations and the
N:P ratio across all species
In this study, the mean root N concentration of the 139 samples
was higher than that reported for the Inner Mongolia grassland of
China by Zhou et al.  and the global data reported by Yuan
et al.  (Table 3). However, the root P concentration of plants
in northern Tibet was slightly lower than that of the Inner
Mongolia grassland of China  but much lower than global
data ; as a result, the root N:P ratio in the northern Tibetan
Plateau was 50% higher than that of Inner Mongolia species 
and 46% higher than the average global data  (Table 3). The
leaf N concentration in our samples was significantly higher than
that found in 753 Chinese plant species by Han et al.  and in
1251 global terrestrial plant species by Reich and Oleksyn , but
lower than that of the Chinese grassland species . Our sampled
plant species had lower leaf P concentrations than those of the
Chinese grassland  and the global averages , but our values
were slightly lower than that of the Chinese flora  The leaf N:P
ratios were 9%, 17% and 29% higher than those in the Chinese
flora , the Chinese grassland  and the global vegetation 
(Table 3), respectively. In conclusion, the northern Tibetan
Plateau samples had a higher N concentration and N:P ratio,
but a lower P concentration.
It is well known that N and P are the major nutrients
constraining plant growth throughout the world [22,23].
Koerselman and Meuleman  showed that a leaf N:P ratio of 14
indicates an N limitation, while a ratio of 16 indicates a P
limitation. The mean value of the leaf N:P ratio in this study was
17.87, which indicated that the plant in the alpine steppe of the
northern Tibetan Plateau was more limited by P, as was shown in
the Chinese flora analysed by Han et al. . One probable
reason for this result is the lower soil P content across China
compared with the global average , and generally plant P
concentration was affected by soil P within the ecosystem .
Moreover, Tian et al.  found that the soil P content in this
frigid highland was even lower than that of the Chinese average.
Because most P input is deposited on the soil surface by
weathering, but gale-force winds (wind speed . 17.2 m N s21)
occurred on more than 100 days per year in this area ; thus,
the nutrient was easily migrated and lost due to low plant cover
and the intense erosion effects of wind . In addition, the
soil on the alpine steppe is alkaline, with a high soil pH and an
abundance of CaCO3 that leads to low P bioavailability .
The leaf N concentration in the cold northern Tibetan Plateau
was significantly higher than the result reported by Han et al. 
and Reich and Oleksyn  (Table 3). The higher N concentration
*, **, and *** represent correlation that is significant at the 0.05, 0.01 and 0.001 level (2-tailed), respectively.
of high-altitude plants may be a result of the inherent
developmental growth constraints inhibiting nutrient dilution in
the plant body . According to Reich and Oleksyn , the
high leaf N concentration offsets the inefficiency of enzymes and
the physiological processes in cold environment, thereby
increasing the metabolic efficiency of plants. At most of our sampling sites
with an MAP below 300 mm and many extremely windy days,
intense evaporation increased the water stress during soil nitrogen
mineralisation and plant growth. This may explain why the leaf N
concentration in alpine steppe was lower than other grassland
types of China , a result of allocating more N to the root to
increase the water absorption capacity with increasing drought
[34,35]. Thus, the root N concentration on the northern Tibetan
Plateau was higher than that in the Inner Mongolia grassland of
China  and higher than global averages .
Across all species, the CVs of root N and P concentrations and
the N:P ratio at our sites were larger than those in the leaves,
indicating that the leaf stoichiometry was more stable than that of
the root (Table 1). The complexity of the root may play a key role
because they have more multistage branches and the structure and
function of each branch is quite different . Root N and P
concentrations were generally less than half of the leaf
concentrations in this study (Table 1), because leaf was the most important
photosynthetic organ requiring high nutrient concentrations to
improve the plants photosynthetic and metabolic capacity .
The N and P concentrations were strongly correlated for the roots
and leaves (Fig. 2. b), and the relationships observed in this study
were similar to those reported by Wright et al. .
Higher leaf nutrient concentrations were accompanied by high
root nutrient concentrations in present study (Fig. 3. a, b). Roots
belong to the structural component and leaves belong to the
metabolic component. The nutrient-rich leaves always exhibited
high photosynthetic and metabolic activity, required
corresponding higher nutrient investments in structural tissue . Because
higher nutrient concentrations in structural tissue may lead to
high rates of nutrient recycling in the phloem, which is linked
closely with increased photosynthate export and phloem loading
Relationship between the N and P concentrations and
the N:P ratio in roots and leaves with climate factors
According to Reich and Oleksyn , the leaf N concentration
increased with the MAT when the temperature was below 5
10uC, because a low MAT limited soil N mineralization, and
reduced soil availability and root-nutrient absorption. However, in
this study, the leaf N concentration of all species in the northern
Tibetan Plateau was unrelated to the MAT (Fig. 5. f). We assumed
that the temperature had no effect on leaf N in cold regions with
an MAT below 0uC, which was consistent with the viewpoint of
He et al. . Even when we combined our leaf N data, the global
data from Reich and Oleksyn , the Chinese data from Han
et al.  and the eastern Tibetan Plateau data from He et al. 
with MAT below 10uC together, no relationship was observed
between the leaf N concentration and the MAT in cold regions
(n = 1392, r = 20.05, P.0.05) (Fig. 6). Why was the leaf N
concentration not sensitive to an increasing MAT under low
temperatures? First, He et al.  argued that phylogenetic
variation (genus) was the key factor that affected the leaf N
concentrations at the biome scale, not climate conditions. Second,
a warming climate may have no effect or a relatively small effect
on soil N availability in alpine and arctic environments during the
growing season . A warming climate may result in
abundant nutrients draining from the thick layer of permafrost
by means of soil water movement (especially in the fallow season)
due to intense freeze-thaw cycles in alpine tundra . Third,
in cold terrestrial ecosystems, low temperature is generally
considered a limiting factor controlling plant growth. Even if the
rising rate of soil N mineralisation could improve root absorption
ability with the temperature increasing, but the increased biomass
could dilute the extra absorption of nitrogen to maintain leaf N
concentrations relatively stable [48,49].
The leaf P concentration was negatively correlated with the
MAT, which was the same trend observed by Reich and Oleksyn
 and Han et al.  (Fig. 5. e, h). A negative relationship
between the leaf P concentration and the MAP was found in this
study (Fig. 5. b). The higher precipitation and temperature could
result in higher rate of rock weathering and more P leaching from
the soil [50,51]. Additionally, due to the inhibiting influence of
cold-adapted phosphatases activities with increasing temperatures,
P immobilisation would increase more rapidly with temperature
than P mineralization; therefore, the dissolved inorganic P released
from alpine and tundra soils was significantly greater at lower
temperature [52,53]. The variation of the leaf P concentration
across the temperature gradient resulted in leaf N:P ratio was
positively correlated with the MAT, which was consistent with the
result of Reich and Oleksyn  (Fig. 5. d, g). Nevertheless, all the
simple linear regression line in our study have gender slopes than
those reported by Han et al.  and Reich and Oleksyn . This
may be caused by the smaller extent of MAT on the northern
Yuan et al.  reported a different pattern of leaf and root N:P
with the latitude (temperature changes) at global scale. Root N:P
declined exponentially, but leaf N:P decreased linearly with the
increasing latitude (decreasing temperature). However, in present
study, the root P concentrations had a negatively linear correlation
with the MAT, and the root N: P ratio also had a positively
correlation with the MAT, which was similar to the result for with
leaves (Fig. 4. d, e; Fig. 5. d, e). Further studies will be required
Chinese grassland 27.6
(Zhou et al. 2010)
*** Significant differences in leaf N and P concentrations and the N:P ratio between the northern Tibetan Plateau and other areas at P,0.001, NS represents no
significant difference in the leaf P content and the N:P ratio between the northern Tibetan Plateau and other areas (P.0.05).
before the conclusions could be made about the differences or
similarities in plant-climate biogeographical variation in root and
We conclude from our observations that correlations exist
between root and leaf N and P with climate factors (MAP and
MAT), even in a particular arctic/alpine environment such as the
northern Tibetan Plateau, which indicates similar evolutionary
strategies and phylogenetic signals to plants in other regions.
However, the temperature-biogeochemical hypothesis (TBH) can
not be used to explain the relationship between plant N
concentrations and MAT in alpine steppe. Our study also
provided a valuable contribution to the global data pool on root
stoichiometry, given the previously limited knowledge on the
alpine plant. Understanding the bio-geographic patterns of root
and leaf nutrients concentrations and the relationships with
climatic factors will aid in modeling ecosystem nutrient cycling
and predicting plant functional traits response to global changes in
high altitude area.
Table S1 Positional information and climate data for
the 32 sites where plant samples were collected.
Conceived and designed the experiments: JTH XDW. Performed the
experiments: JTH JBW. Analyzed the data: JTH XDW. Contributed
reagents/materials/analysis tools: JTH JBW. Wrote the paper: JTH XDW.
Figure: JTH JBW. Revised the manuscript: XDW JTH JBW.
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