Soil, Leaf and Root Ecological Stoichiometry of Caragana korshinskii on the Loess Plateau of China in Relation to Plantation Age
Soil, Leaf and Root Ecological Stoichiometry of Caragana korshinskii on the Loess Plateau of China in Relation to Plantation Age
Quanchao Zeng 1 2 3
Rattan Lal 0 1 3
Yanan Chen 1 2 3
Shaoshan An 1 2 3
0 Carbon Management and Sequestration Center, The Ohio State University , Columbus , Ohio, United States of America, 3 State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University , Yang ling, Shaanxi , China
1 Funding: This study was supported by the National Natural Science Foundation of China (41671280, 41171226) and the non-profit Industry Research Project of Chinese Ministry of Water Resources , 201501045
2 College of Natural Resources and Environment, Northwest A&F University , Yangling , P.R. China
3 Editor: Dafeng Hui, Tennessee State University , UNITED STATES
Caragana korshinskii, a leguminous shrub, a common specie, is widely planted to prevent soil erosion on the Loess Plateau. The objective of this study was to determine how the plantation ages affected soil, leaf and root nutrients and ecological stoichiometry. The chronosequence ages of C. korshinskii plantations selected for this study were 10, 20 and 30 years. Soil organic carbon (SOC) and soil total nitrogen (STN) of C. korshinskii plantations significantly increased with increase in the chronosequence age. However, soil total phosphorous (STP) was not affected by the chronosequence age. The soil C: N ratio decreased and the soil C: P and N: P ratios increased with increasing plantation age. The leaf and root concentrations of C, N, and P increased and the ratios C: N, C: P, and N: P decreased with age increase. Leaf N: P ratios were >20, indicating that P was the main factor limiting the growth of C. korshinskii. This study also demonstrated that the regeneration of natural grassland (NG) effectively preserved and enhanced soil nutrient contents. Compared with NG, shrub lands (C. korshinskii) had much lower soil nutrient concentrations, especially for long (>20 years) chronosequence age. Thus, the regeneration of natural grassland is an ecologically beneficial practice for the recovery of degraded soils in this area.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Competing Interests: The authors have declared
that no competing interests exist.
Ecological stoichiometry is the study of the balance of energy and multiple chemical elements
in ecological interactions [
]. Ecological stoichiometry connects evolutionary patterns
affecting organismal elemental compositions to large-scale consequences and constraints associated
with energy and material flows in ecosystems [
]. Ecological stoichiometry, especially for
carbon (C), nitrogen (N) and phosphorus (P), plays an important role in analyzing composition,
structure and function of a concerned community and ecological system [
]. It has been used
in different different systems to explore the limited nutrition for varied plant groups [2, 4±9].
Generally, green leaf N:P ratio can indicate plant nutrition limitation, providing suggestive
guide to the practice of vegetation management [3, 9±11]. Leaf N:P ratio (mass ratio) has been
suggested to be useful for indicating the shift between NÐand P -limitation [
based on fertilization experiments proposed that low leaf N:P ratios (<14) reflect N limitation,
that high N:P ratios (>16) likely reflect P limitation[
3, 13, 14
]. This threshold value has been
widely used in different ecosystems.
Vegetation restoration is an effective and beneficial soil conservation practice that can
enhance the contents of soil nutrients [
]. The Loess Plateau was the largest eroded land
area of China . In 1999, the Chinese government initiated the ªGrain for Greenº program
to address the environmental and economic developmental problems[
]. The program is
aimed at converting degraded farmland into forest, shrub, and grassland [
grasslands such as the Yunwu Mountain have been protected by establishing shrub land and
forest land over large areas [
]. Vegetation restoration has improved soil quality over the
last 30 years. Vegetation succession increases small macro-aggregates, bulk soil carbon(C) and
aggregate C with an increase in duration of the plantation [
]. Wang et al. (2015)
reported that after 15 years of conversion, the natural restoration process must be utilized
properly to enhance the accumulation of soil organic carbon (SOC) upon conversion from
cropland to grassland. Research studies thus far indicate that vegetation restoration strongly
impacts soil quality and the attendant ecosystem services.
C. korshinskii is the most common shrub which had been established over large areas on
the Loess Plateau. Because most studies concerning soil nutrients and aggregate stability in
this area, little is known about C:N:P stoichiometry in Caragana korshinskii leaf, roots, and soil
under different duration age. The duration of the establishment of this shrub varies between
10 and 30 years. Therefore, it is pertinent to assess variations in soil, leaf and root ecological
stoichiometry with changes in duration of the plantation. These results will provide well
understanding of the practice of planting Caragana korshinskii from ecological stoichiometry
aspect. In this study, we focused on C. korshinskii along a successional gradient and a natural
grassland with 30 duration years in northwest China. Previous studies had showed that
duration age had positive on soil nutrients, especially for the storage of carbon and nitrogen in the
grassland [23±25]. Based on the previous studies, we addressed following hypotheses: (1)
plantation ages had the positive effects on soil nutrients and ecological stoichiometry; (2) natural
restoration might be better method to improve soil nutrients compared with establishing C.
korshinskii for the limited precipitation in drylands.
Materials and Methods
C. korshinskii areas were located in the Shanghuang watershed (106Ê260±106Ê300 E, 35Ê590±36Ê
020N) in the Loess Plateau, Ningxia province of China, which covered an area of 8.19 hm2.
This region had a semi-arid climate. The average annual temperature (MAT) was 6.9ÊC and
the average annual precipitation (MAP) was about 419 mm (1982±2002 data) [
]. A severe
decline in soil quality and accelerated erosion, serious threats to human wellbeing, were
attributed to decline in the vegetative cover because of over-gazing, intensive cultivation and other
anthropogenic perturbations. Towards an attempt to address the environmental and economic
developmental issues, Shanghuang watershed had been used to conduct restoration projects.
Thus, vegetation restoration had been attempted by establishing C. korshinskii. Thus, the most
popular shrub had been planted in the watershed over a wide range of duration. The watershed
was highly diverse physiographically and in terrain characteristics spatially (90% of the area is
covered by hills, 51% of the land is located at altitude of 1534.3±1822.0 m, and the terrain was
closely dissected and sharp-edged with steep slopes) [
]. Restoration of vegetation since circa
1984 had strongly changed the watershed into a demonstration zone for successful land
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reclamation and comprehensive management. Therefore, the sampling sites for this study
ranged in age duration for 10, 20 and 30 years since the establishment of C. korshinskii plantations
after imposing the grazing exclusion.
Another sample site was a natural grassland in the same area, which was a control
experiment to compare the effects of vegetation restoration between shrub land and natural
grassland. The two sample areas had similar climate (MAP and MAT) and soil types (Entisols, U.S.
A. taxonomy). Natural grassland was selected ªYunWu Mountain Nature Reserveº where was
near Shanghuang watershed. It had a well-protected Stipa bungeana population, with an area
of 6700 ha, an altitude of 1800±2100 m and an MAT of 6±7ÊC. The MAP is 455 mm, most of
that occurred during the summer (from June to September). In this area, most plants were
herb with natural succession, with the constructive species of Stipa bungeana and Stipa grandis.
Other companion species were Thymus mongolicus, Potentilla bifurca, Artemisia vestita,
Agropyron dasystachys, Heteropappus altaicus, etc [
We state that no specific permissions were required for these locations/activities. We
conform that the field studies did not involve endangered or protected species.
Sampling and analyses
We chose three different ages of plots of C. korshinskii and a natural grassland site without
human disturbance as a control which could compare the differences of C. korshinskii land
and grass land duration on soil nutrients and ecological stoichiometry. There were three field
plots for every site as repeats. Three subplots (20 × 20 m) were established for each plantation
age and NG site, with a total of 36 subplots. In each subplot, we collected three soil and plant
samples, respectively. The dominant species and geographic information in each sampling site
were showed in Table 1.
In natural grassland, we just collected soil samples. Thus, a total of 72 soil samples (under
C. korshinskii and NG), and 54 samples of each of root and leaf for only of C. korshinskii were
collected in this study area in mid-August 2014. Soil and plant samples were collected as
previous studies descripted [
]. Briefly, five soil cores (0±20 cm and 20±40 cm depths) were
collected from each quadrat using a 3-cm diameter soil auger and mixed to obtain a composite
sample. After removing stones, roots and small animals, soil samples were air-dried and sieved
through a 0.15 mm sieve for the analysis of soil organic carbon, total nitrogen and total
phosphorus. Plant samples included green leaf and root samples. In each subplot, we collected
green leaf and root from 5 well-grown C. korshinskii. All the roots were fine roots with the
diameter of < 0.5 mm. Leaf and root were watering with distilled water and dried at 65ÊC for
about 72 hours until reached a consistent weight. After over-dried, leaf and root samples
grounded using a ball mill and sieved through a 0.15 mm sieve.
Concentrations of total nitrogen (TN) of the plant tissues and of soil total nitrogen (STN)
were determined colorimetrically using the Kjeldahl acid-digestion method (KDY-9830) after
extraction with 0.02 mol/L sulfuric acid [
]. Total plant P (TP) was measured using
colorimetric analysis (UV 2800) after digestion with H2SO4 and H2O2 [
]. Soil total P (STP) was
measured using a spectrophotometer after wet digestion with H2SO4 and HClO4 followed by
colorimetric analysis (UV 2800) [
]. The organic C concentration in soils and plants was
measured using a modified Mebius method [
]. More specifically, 0.5 g of soil samples (or
0.02 g of plant samples) were digested with 5 ml of 1 mol/L K2Cr2O7 and 5 ml of concentrated
H2SO4 at 180ÊC for 5 min, followed by titration with standardized FeSO4 (0.2 mol/l).
We used one-way analysis of variance (ANOVA) to analyze the effects of duration age on
nutrients and stoichiometric characteristics of the soil, root, leaf. Linear regression analysis
was used to test the relationships between the soil and plant stoichiometric characteristics. All
the significant differences were showed at the level of 0.05. SPSS 20.0 software (SPSS, Inc.,
Chicago, IL, USA) was used for the statistical analysis. Soil and plants nutrients concentrations
expressed as g/kg on a dried weight basis and all the C:N:P ratios were mass ratios. Figures
were conducted by Origin 9.0.
Soil nutrients and soil C:N:P characteristics
The plantation age had significant effects on the soil organic carbon (SOC) and soil total N
(STN) concentrations (Fig 1). Concentrations of SOC (g/kg) for 10, 20 and 30 yr duration
were 10.79, 12.66 and 13.85 in the 0-20-cm soil layer compared with 8.13, 8.49, and 8.97 in
2040-cm layer, respectively. Concentrations of STN increased with increase in the plantation age,
and the highest value was measured at 30 yr. Concentration of STN (g/kg) for 30 yr was, 1.57
and 1.05 in 0±20 cm and 20±40 cm-soil layer, respectively. In comparison, concentration of
STP had a narrow range (0.46±0.50 g/kg) in 0-20-cm and 20-40-cm soil layers. While
concentrations of SOC and STN changed significantly (P<0.05) with increase in the plantation age
(from 10 yr to 30yr), that of STP had no significant effect. However, concentrations of SOC
and STN under NG were approximately 2-fold higher than those measured under C.
korshinskii plantations. Similarly, concentration of STP under NG was much higher than that
measured under three C. korshinskii sites of 10 yr, 20 yr, and 30yr.
The soil ecological C:N:P stoichiometry also varied with the plantation age (Fig 1). The soil
C:N ratios for plantation age of 10, 20 and 30 yr under C. korshinskii were 9.12, 9.07, and 8.80
in the 0-20-cm soil layer, respectively. However, the C:N ratio was rather narrow (8.51±8.59)
in 20-40-cm layer. Overall, along the plantation age significantly impact the soil C:N ratio. In
fact, the trend of the soil C:P ratio was also similar to that for soil N:P ratio (Fig 1). The soil N:
P ratio significantly increased with increase in the plantation age for both soil depths (Fig 1).
The C:N:P ratio also increased with increase in the plantation age (Table 2).
Leaf and root C, N and P contents and C:N:P characteristics
The plantation age had a significant effect on leaf total C, total N and total P concentrations.
The highest concentrations (g/kg) of total C (475.2), total N (42.3) and total P (1.9) were
observed under the 30-year-old and the lowest under 10-year-old plantation of C. korshinskii
(Fig 2). Concentration (g/kg) of nutrients in roots ranged from 452.3 to 466.3 for total C, 21.2
to 27.0 for total N, and 1.6 to 1.9 for total P.
Increase in the plantation age decreased the ratio of nutrients in the leaves from 12.0 to 11.2
for C:N, 291.3 to 247.1 for C:P, and 24.3 to 22.0 for N:P. Trends in the ratio of nutrients in the
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Fig 1. Stoichiometric characteristics of soil C, N and P as affected by soil depth and plantation age. Values are the
means ± SE of three plots. Values designated by different lowercase letters were significantly different among different
duration ages, and different capital letters indicated significant difference soil layers, respectively (P < 0.05).
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roots with regards to the planation age for C:N, C:P and N:P exhibited trends similar to those
of the leaves. The plantation age had a significant effect on the leaf and root ecological
The highest leaf C:N:P ratios were observed in the 30-year-old and the lowest in the
10-year-old plantation (Table 2). Trends of the root C:N:P ratios were similar to those of the
leaves (Table 2). In general, the plant C:N:P ratios increased with increase in the plantation
Relationships between soil versus leaf and root stoichiometry
The leaf C:P ratio decreased linearly with the soil C:P ratio (r = -0.925, P<0.01 for the
020-cm; r = -0.736, P = 0.024 for 20-40-cm layer) (Fig 3b). The N:P ratio in soil under C.
korshinskii varied linearly with the leaf N:P ratio (r = -0.905, P<0.01 for the 0-20-cm; r = -0.768,
P = 0.016 for 20-40-cm layer) (Fig 3c). In the 0-20-cm layer, the soil C:N ratio increased
linearly with the root C:N ratios (r = 0.768, P = 0.016) (Fig 3d). The soil N:P ratios decreased
linearly with the root N:P ratios (r = -0.945, P<0.01 for 0-20-cm; r = -0.826, P = 0.006 for
2040-cm layer) (Fig 3e). The soil C:P ratios decreased linearly with the root C:P ratios (r = -0.974,
P<0.01 for 0-20-cm; r = -0.868, P = 0.002 for 20-40-cm layer) (Fig 3f).
The effects of plantation ages of C. korshinskii
Vegetation restoration was one of the most effective method to solve the soil erosion problem,
especially on the Loess Plateau of China [
]. Shrubs (i.e. C.korshinskii) were one of the
most common vegetation types in the Shanghuang watershed and had been used to improve
the soil quality, including soil aggregates and nutrient availability. The data from the present
study showed that vegetation age had positive effects on soil nutrients, and these results were
in accord with those reported for the Shapotou area , Yaoledianzi village in northeast
], Wulanaodu area in northeast China [
], and Yanchi country in Ningxia province,
northwest China [
]. Revegetation from abandoned farmland significantly influenced soil
total C and total N, resulting in a C:N ratio of about 10 after 30 years of abandonment [
The observations in this study showed that the C:N ratio of soil under C. korshinskii ranged
from 8.80 to 9.11. In the first 20 years, soil C:N ratio was nearly constant, and significant higher
than the soil in the duration of 30 years. Soil total C concentration was significantly correlated
with the soil total N, indicating similar trends for soil C and N storage. This coupling relation
led to a narrow range for soil C:N ratio.
The N: P ratio in leaf was an indicator of N or P limitation in terrestrial ecosystems [
relationships between leaf N: P ratios and plant properties have also been used to indicate their
responses to environmental change or human disturbance [
]. In this study, the N:P ratios
decreased with increase in plant age, and all the ratios were higher than 20. Review of previous
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Fig 2. Stoichiometric characteristics of leaf and root C, N and P as affected by plantation age. Values are the
means ± SE of three plots. For each plant issue, means with different letters are significantly different based on ANOVA and
Scheffe's test (P<0.05). Note: Values designated by different lowercase letters were significantly different among different
duration ages, and different capital letters indicated significant difference between leaf and root, respectively (P < 0.05).
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Fig 3. Relationships between soil, leaf and root stoichiometric characteristics of C.korshinskii.
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], showed that C. korshinskii was limited by P nutrition, and the severity of
limitation decreases with the increase in age of the shrub, implying that older C. korshinskii plants
need a much lower available P requirement for growth. Therefore, soil available P content
would increase strongly with increasing C. korshinskii age, and which had positive
consequences for soil quality. However, it was interesting that soil total P concentration was not
decreased with age increase. Because soil parent materials were the main resources of total P
content. Thus C. korshinskii soil total P had no significant changes with age increase.
The difference between C. korshinskii and natural grassland
Land use was another factor affecting soil nutrients. Grasslands played an important role in
the global C and N cycles. The data showed that soil total C and total N were higher in the
older grasslands (30 years) and the values were much higher than in a soil with similar aged C.
korshinskii plots. Thus, vegetation type had a strong effect on the soil C and N storage. Li et al.
] reported that C input was greater than C output in an enclosed grasslands. Soil N
fixation by C. korshinskii and subsequent N released by litter decomposition could increase
soil N content [
]. Carbon fixation via photosynthesis and the subsequent transfer of C to the
soil via leaf, litter and root turnover contributes to soil C accumulation [
]. A larger
aboveground biomass indicated that more litters returned to the soil and the roots exudates would
contain more nutrients.
At the same age, soil under natural grassland had the highest total C, total N and total P,
suggesting that, compared with natural grassland, C. korshinskii was not the most suitable
specie for restoration of eroded lands in this region. Firstly, C. korshinskii required more amount
of water and nutrients to maintain its growth than grasses for the higher living biomass.
Secondly, given that plant growth was main limited by water in the dryland [
], the annual
precipitation was limited in this area. Finally, soils of the studied areas were deficit in nutrients
before planting C. korshinskii because of over grazing, which also limited the growth of C.
korshinskii. Therefore, natural restoration may be the best approach to restore degraded soils to
attain the desired outcome albeit taking a long time. While establishing C. korshinskii
improved soil quality over a short time period, it had negative effects on the soil on the
longterm basis. Consequently, planting C. korshinskii was not the best choice to improve soil
quality for Shanghuang watershed in the long run.
C. korshinskii, a leguminous shrub, is a dominant native plant species that is widely planted to
prevent soil erosion on the Loess Plateau. The results showed that C. korshinskii growth altered
concentration of nutrients in soil, leave and root. The leaf N:P ratios were higher than 20
regardless of the age of the shrub. Therefore, the growth of C. korshinskii was limited by P
availability. Compared with natural grassland, planting Caragana korshinskii scrubland may
not be a good choice for vegetation restoration as its soil fertility was lower than the natural
grasslands. Accumulation of soil nutrients under C. korshinskii is a slow process and takes a
S1 File. Supporting information about data.
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This study was supported by the National Natural Science Foundation of China
(41671280,41171226) and the Non-profit Industry Research Project of Chinese Ministry of
Water Resources (201501045). We also thank the anonymous reviewers and editor for their
great help in improving the quality of the manuscript.
Conceptualization: SA RL.
Data curation: QZ.
Formal analysis: QZ YC.
Funding acquisition: SA.
Investigation: QZ YC.
Methodology: QZ YC SA.
Project administration: QZ SA.
Resources: SA RL.
Software: YC QZ.
Validation: QZ RL.
Visualization: YC SA.
Writing ± original draft: QZ YC.
Writing ± review & editing: RL SA.
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