Global Ecology and Conservation 38 (2022) e02202

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Global Ecology and Conservation

journal homepage: www.elsevier.com/locate/gecco

Ecosystem photosynthesis depends on increased water availability

to enhance carbon assimilation in semiarid desert steppe in
northern China
Jianfei Yu a, Yi Zhang a, Yutao Wang a, Xu Luo a, Xiaoqian Liang a, Xumei Huang a,
Yaxin Zhao a, Xinyang Zhou a, Jianping Li a, b, *
a
College of Agriculture, Ningxia University, Yinchuan 750021, China
b
State Key Laboratory Cultivation Base for Northwest Degraded Ecosystem Recovery and Reconstruction, Yinchuan 750021, China

A R T I C L E I N F O A B S T R A C T

Keywords: The amount and intensity of precipitation may have important effects on plant growth and ecosystem
Carbon cycling carbon exchange in semiarid desert steppes; further understanding of how the dryland carbon cycle
Ecosystem respiration responds to changes in precipitation and its underlying mechanisms is necessary for an accurate
Soil respiration
understanding of the global carbon cycle. A field experiment was conducted in a semiarid desert
Simulated precipitation
steppe in Ningxia, China, to clarify the response patterns of ecosystem carbon fluxes along five levels
Semiarid grassland
of precipitation gradients (Simulating the natural precipitation percentages of 33 % (− 33 %, 84 mm),
66 % (− 66 %, 167 mm), 100 % (CK, 253 mm), 133 % (+33 %, 336 mm) and 166 % (+66 %, 420
mm) by rain shelters and sprinklers; CK is natural precipitation). The result showed that the trends of
net ecosystem CO2 exchange (NEE) and gross ecosystem photosynthesis (GEP) were consistent and
those of ecosystem respiration (ER) and Soil respiration (SR) and autotrophic (Ra) and heterotrophic
(Rh) components of SR were also consistent. NEE, ER, GEP and SR all reached their highest values in
August. Changes in precipitation significantly affected ecosystem carbon fluxes, with NEE, ER and SR
decreasing with decreasing precipitation and NEE, ER and GEP increasing with increasing precipi­
tation. Soil respiration was more sensitive to the decreased precipitation treatment. During the
growing season, NEE, ER, GEP, and SR were significantly positively correlated with precipitation, soil
moisture (SM) and aboveground biomass (AGB). With the increase of precipitation variability, the
promotion effect of increasing precipitation on GEP will exceed the promotion effect on ER, causing
changes in carbon exchange and carbon sinks. Photosynthesis and respiration appeared tightly
coupled, indicating that photosynthetic products regulate above- and belowground carbon cycling in
semiarid steppe. Our study highlights the importance of water availability in carbon exchange
processes in semiarid desert steppe of northern China. Decreased precipitation can lead to significant
changes in SM and AGB, with negative impacts on GEP and SR, resulting in uncertainty in regional
carbon sequestration. These findings will help us understand the vulnerability of semiarid steppe
ecosystems under the influence of future precipitation changes and aim to provide a scientific
reference for ecological management and restoration of semiarid desert steppes.

* Correspondence to: Agricultural College of Ningxia University, Yinchuan City, Ningxia Hui Autonomous Region 750021, China.
E-mail addresses: yjf17899318859@163.com (J. Yu), 13995378736@163.com (Y. Zhang), 18234171762@163.com (Y. Wang), luoxu181226@
163.com (X. Luo), laic5975@163.com (X. Liang), 19995394027@163.com (X. Huang), zyxtt1026@163.com (Y. Zhao), 12021131325@stu.nxu.edu.
cn (X. Zhou), lijianpingsas@nxu.edu.cn (J. Li).

https://doi.org/10.1016/j.gecco.2022.e02202
Received 7 April 2022; Received in revised form 7 June 2022; Accepted 18 June 2022
Available online 21 June 2022
2351-9894/© 2022 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/by/4.0/).
J. Yu et al. Global Ecology and Conservation 38 (2022) e02202

1. Introduction

As an important material cycling process linking the biosphere and the atmosphere, terrestrial ecosystem carbon cycle processes are
key to the prediction of future changes in atmospheric CO2 and other greenhouse gas concentrations (Knapp and Smith, 2001).
Terrestrial ecosystem carbon cycle processes mainly include the process of atmospheric CO2 uptake by gross ecosystem photosynthesis
(GEP) and the process of CO2 release due to ecosystem respiration (ER) (Zhang et al., 2019; Xia et al., 2009), while GEP and ER together
determine net ecosystem CO2 exchange (Li et al., 2017). The net ecosystem carbon exchange (NEE) represents the net carbon uptake
capacity, the size of a terrestrial ecosystem’s NEE determines its capacity to store carbon, and the specific ecosystem net carbon ex­
change depends on the balance between carbon uptake and carbon release (Yang et al., 2022). Soil respiration (SR), the largest
contributor to ER, and its carbon cycling processes have been a popular topic of ecological research (Li et al., 2021). As an important
carbon cycle pathway linking the soil carbon pool to the atmospheric carbon pool, changes in soil respiration can significantly affect
terrestrial carbon exchange and hence the global climate (Dhaliwal et al., 2019).
Grasslands, as one of the most widely distributed terrestrial ecosystems in the world, accounting for 32 % of the global natural
vegetation area and storing 34 % of the carbon of global terrestrial ecosystems (Ghosh and Mahanta, 2014). In addition, grasslands
worldwide are predominantly found in ecologically sensitive areas, particularly arid and semiarid regions, where they have short life
cycles, rapid renewal rates, and relatively fragile productive capacity and are more sensitive to climate change than other terrestrial
ecosystems, particularly changes in precipitation patterns (Knapp and Smith, 2001), which will directly affect grassland net primary
productivity and carbon cycling in grasslands (Knapp et al., 2002). A recent study by Ahlström et al. (2015) suggests that the carbon
sequestration capacity in semiarid ecosystems will determine interannual fluctuations in the global carbon cycle under future climate
change scenarios. Thus, arid and semiarid ecosystems may play an important role in future feedbacks to the terrestrial carbon cycle and
climate change (Chen et al., 2009).
Global climate studies have shown that warming is often accompanied by changes in precipitation patterns (Alexander et al., 2013).
Changing precipitation patterns are mainly manifested in changes in precipitation intensity, frequency and seasonal distribution
(Wentz et al., 2007). Steppe ecosystems are primarily influenced by water availability (Christensen et al., 2004), and as water is
essential for most ecological processes, such as plant growth and microbial activity, changes in precipitation patterns will inevitably
affect all aspects of the ecosystem carbon cycle (Wenninger and Inouye, 2008), particularly in arid desert steppe areas. In
moisture-limited semiarid grassland ecosystems, many studies have found a significant positive correlation between precipitation and
carbon exchange. For example, studies in semiarid steppe ecosystems of Inner Mongolia found that increased growing season pre­
cipitation increased net carbon uptake (Niu et al., 2008) and soil carbon respiration (Liu et al., 2009). A 7-year study in a Canadian
boreal poplar forest found that NEE increased significantly under drought conditions even though ecosystem respiration and total
ecosystem photosynthesis were both significantly reduced (Griffis et al., 2004). This is mainly because ecosystem respiration may be
reduced more under drought conditions than total ecosystem photosynthesis. A 9-year study on semiarid steppes in China found that
the rate of change of ER was greater than that of GEP under the same precipitation conditions, resulting in a significant decrease in
NEE; but as precipitation increased during the growing season, the rate of change of GEP exceeded that of ER, resulting in a significant
increase in NEE (Li et al., 2017). This suggests that the sensitivity of the dryland carbon cycle to increased and decreased precipitation
is not symmetrical (Knapp and Smith, 2001). A meta-analysis of the effects of precipitation changes on carbon cycling processes in
steppe ecosystems also showed that ecosystem photosynthesis, ecosystem respiration, and net primary productivity had higher
sensitivity to increased precipitation (Wu et al., 2011). In addition, another meta-analysis examining the effect of precipitation changes
on soil carbon fluxes reported that soil respiration was more sensitive to increased rainfall in dry areas and to reduced precipitation in
wet areas. Climatic factors such as changes in precipitation will significantly affect fluxes in terrestrial ecosystems (Chen et al., 2009;
Sun, 2017), and precipitation can regulate plant photosynthesis and microbial activity by altering the availability of soil water and
nutrients and directly affect carbon exchange processes in plant–soil systems (Zhu et al., 2021).
In the context of climate change, it is still unclear how changes in precipitation will affect the relationship between total ecosystem
photosynthesis and respiration for most dryland ecosystems where water limitation is more severe (Li et al., 2021). To some extent,
existing studies have rarely considered measuring plant photosynthesis and soil CO2 emissions simultaneously, resulting in a lack of
theoretical knowledge. Soil respiration consists of two main components, CO2 released from plant root metabolism (autotrophic
respiration, Ra) and CO2 released from soil microorganisms (heterotrophic respiration, Rh). Both processes are regulated by soil
moisture, temperature and carbon substrates (Han et al., 2017; Su et al., 2020). The substrate for root respiration is mainly derived
from photosynthesis, and changes in photosynthesis will directly affect root respiration (Kuzyakov and Cheng, 2001). It has been
suggested that changes in water availability due to decreased precipitation may reduce photosynthesis and thus autotrophic respi­
ration (Wertin et al., 2016). However, when the water limitation is alleviated through increased precipitation, subsurface carbon
allocation to the GEP will be reduced due to the reduction in the carbon substrate required by plant roots and soil microbes to obtain
water from the soil, which will also reduce microbial heterotrophic respiration (Suseela and Dukes, 2013). Thus, the balance of carbon
fluxes between photosynthesis and respiration and the coupling between the two will depend on the response to environmental change
(Larsen et al., 2007). How these factors will be superimposed in response to global climate change is uncertain.
Beginning in June 2018, a field experiment manipulating precipitation was initiated on a desert steppe in northern China to study
the effects of precipitation quantity and precipitation intensity on carbon fluxes in semiarid steppe ecosystems. We aim to address the
following three questions: 1) How will changing the amount and intensity of precipitation affect seasonal ecosystem carbon fluxes? 2)
Whether changes in carbon fluxes due to changes in precipitation are attributable to responses of biotic and abiotic factors to changes
in moisture. 3) How will the relationship between above- and below-ground fluxes respond to changes in precipitation?

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2. Materials and methods

2.1. Site description

The study site is located in the desert steppe of Sidunzi Ecological Field Station, Yanchi County, Ningxia, China (107◦ 25´E, 37◦ 47´N,
1431 m above sea level). In the geographical unit, it is connected to the Maowusu Desert to the north and the Loess Plateau to the
southeast, which belongs to the transition zone from the loess hilly to Ordos platform, and the whole county transitions from steppe to
desert steppe from southeast to northwest. The region has a typical temperate continental monsoon climate. The long-term
(1981–2020) mean annual precipitation in the local area is less than 300 mm, with 80 % distributed between July and September.
The mean annual air temperature is 9.1 ℃, and the average temperatures in January and July are − 7.5 ◦ C and 23.5 ◦ C, respectively
(Fig. 1). The soil types in the study region are mainly lime zebra soil, followed by aeolian sandy soil and black loam soil. The main
natural plant species include Agropyron mongolicum, Polygala tenuifolia, Lespedeza potaninii, Peganum harmala, Oxytropis racemosa,
Artemisia scoparia and Stipa reviler (An et al., 2019).

2.2. Experimental design

The experiment used a one-way completely randomized design, leading to a total of 15 plots, and each plot was 6 × 6 m in size. The
distances between different plots are greater than 5 m. Based on the 37-year (1981–2017) average precipitation and extreme fluc­
tuations in the study area, we set five levels of precipitation gradients, which are 33 % (− 33 %), 66 % (− 66 %), 100 %(CK), 133 %
(+33 %), and 166 % (+66 %) of natural precipitation (CK is natural precipitation), respectively. And each treatment was repeated
three times. Based on the average precipitation in the study area during the field experiment period (2018.6–2021.9), the five levels of
precipitation treatments corresponded to experimental period precipitation of 84 mm (33 %), 167 mm (66 %), 253 mm (CK), 336 mm
(133 %) and 420 mm (166 %), respectively (Fig. 2, Table A.1). We simulated the precipitation treatment by using artificial rain control
devices (rain shelters and sprinklers). Multiple concave transparent plexiglasses (made of polycarbonate material that allows 90 % of
the photosynthetically effective radiation to pass through it) were placed on a metal steel frame 2.5 m above the soil surface and set on
each plot of reduced rainfall, sheltering 33 % and 66 % of the natural precipitation, respectively (Fig. 3a). For increasing precipitation
treatment, we calculated 133 % and 166 % corresponding to precipitation by measuring the precipitation in the rainfall collection
device (plastic container) after each rainfall event, and manually added 133 % and 166 % of natural precipitation using sprinklers in
the treatment plot corresponding to 133 % and 166 %, respectively, within 48 h after the precipitation event, without changing the
frequency of natural precipitation. In addition, we isolated water diffusion around each plot with 1.1 m high plastic sheets buried at a
depth of 1.0 m below ground and exposed 10 cm above ground to prevent surface runoff (Fig. 3b). The soil respiration and ecosystem
carbon exchange were measured as show in Fig. 3c and d.

2.3. Measurements of ecosystem carbon fluxes

Three years after precipitation treatment, we completed all measurements in the fourth year (May-October 2021) of the growing
season. Ecosystem CO2 exchange was measured by placing a square aluminum frame (50 × 50 cm, 5 cm high, 3 cm embedded in soil)
inside each plot. In addition, we measured soil respiration (SR) and soil heterotrophic respiration (Rh) by placing two PVC collars
(20 cm in diameter, 50 cm apart) next to each aluminum frame. The PVC collars used to measure SR were 5 cm in height and 3 cm into
the soil, while the PVC collars used to measure Rh were 50 cm in height and 45 cm into the soil. We used gap analysis to measure Rh
(Ohashi et al., 2000), i.e., a larger area was cleared of aboveground vegetation before placing the PVC collar, and because the root
system of most plants are distributed in the topsoil layer (0–30 cm), the 45 cm PVC collar both cut off the roots of existing soil plants
and prevented the growth of new roots within the PVC collar. Carbon fluxes were measured using two infrared gas analyzers (LI-6800

Fig. 1. Average monthly precipitation and temperature (1981–2020).

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Fig. 2. Performance of the experimental setup. The rainfall manipulation resulted in statistical precipitation treatments in 2018, 2019 and 2020 by
mapping on the estimated probability density curve based on historical precipitation data (1981–2020).

portable photosynthesis system and Li-8100 automated soil CO2 flux system; Li-COR, Lincoln, NE, USA) (Fig. 3c-d). For the mea­
surements, a transparent chamber (0.5 × 0.5 × 0.5 m3) with a thickness of 6 mm and 99 % light transmission was fixed on an
aluminum frame inserted 3 cm into the soil to ensure that it constituted a closed gas sampling chamber and connected to the LI-6800.
Meanwhile, a cooling fan was installed on the side and top of the transparent chamber to mix the gas in the chamber, and after the gas
reached a steady state for 20 s, the CO2 concentration was continuously recorded for 90 s, from which the NEE was calculated (Li et al.,
2017; Xia et al., 2009). After measuring NEE, the lift the transparent chamber and put it back on the base when the CO2 and H2O
concentrations in the chamber are close to the external values, and cover it with an opaque black cloth, and the above measurement
was repeated. Since the second measurement was made with a blackout cloth, photosynthesis was excluded, and the calculated value
was ER. GEP was calculated as GEP = ER – NEE. (Li et al., 2017; Zhang et al., 2019). This static chamber approach has been suc­
cessfully used to assess ecosystem fluxes (Niu et al., 2008; Xia et al., 2009). SR and Rh were measured using a Li-8100. To avoid soil
respiration being affected by plant aboveground respiration, the aboveground parts of plants were removed from the PVC collar the
day before the measurement. Autotrophic respiration (Ra) was obtained from the difference between soil respiration and heterotrophic
respiration. NEE, ER, SR, and Rh were measured simultaneously from 9:00–11:30 a.m.

2.4. Soil characteristics and plant biomass

From May to September 2021, soil temperature (ST) at 5 cm and soil moisture (SM) at 10 cm were measured using a thermocouple
temperature probe and moisture detector carried by Li-8100 (Li-Cor, USA) in parallel with soil carbon emission measurements.
Biomass reached its maximum in late August, and we selected a representative sample of the areas vegetation within each plot for
vegetation survey (sample size 1 × 1 m) and sample collection. After the vegetation survey, all plants in each sample square were cut
off flush with scissors and brought back to the laboratory. The collected fresh samples of plants were dried at 70 ◦ C for approximately
48 h and then weighed to determine the plant aboveground biomass (AGB).

2.5. Statistical analysis

Repeated-measures ANOVA was used to assess the effects of precipitation, sampling date, and their interactions on NEE, GEP, ER,
and SR (including Ra and Rh). One-way ANOVA was used to test for differences between precipitation treatments for ecosystem carbon

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Fig. 3. Field experiment design and ecosystem carbon flux measurements. a) precipitation gradient control device; b) Block surface runoff; c)
Measurement of soil respiration (SR); d) Measurement of carbon fluxes (NEE and ER).

fluxes, and post hoc multiple comparisons (LSD) were performed if the differences were significant (P < 0.05). The relationships
between ecosystem carbon fluxes and SM, ST, precipitation and AGB were investigated using linear regression equations. The effects of

Fig. 4. Effects of decreased precipitation (84 mm and 167 mm), control (natural precipitation, 253 mm), and increased precipitation (336 mm and
420 mm) on soil temperature (ST, a) at 5 cm depth and soil moisture (SM, b) at 10 cm depth.

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NEE, ER, GEP and SR due to the precipitation gradient were defined as follows: percentage effect = ((precipitation treatment – control)
/ control) * 100 (Zhang et al., 2017; Zhang et al., 2019). We used the mean ecosystem carbon fluxes for each month to calculate the
seasonal mean ecosystem carbon fluxes, and the data are expressed as the mean ± standard error. SPSS 22.0 (SPSS Inc., Chicago, IL,
USA) was used for statistical analysis of all data. Graphs were plotted using Origin 2021 (OriginLab Corporation, USA).

3. Results

3.1. Variations in precipitation, soil moisture, soil temperature and plant biomass

Changes in precipitation during the 2018–2021 field experiment are shown (Fig. 2, Table A.1). Along five levels of precipitation
gradients, precipitation increases from 96 mm, 106 mm, 66 mm, and 75 mm under the 33 % precipitation treatment to 485 mm,
536 mm, 334 mm, and 377 mm under the 166 % precipitation treatment from 2018 to 2021, respectively, and throughout the growing
season (May-September) in 2021, precipitation ranged from 40.4 mm to 203.2 mm.
Throughout the growing season, precipitation did not significantly change the soil temperature (ST) at 5 cm depth (Fig. 4a), while
changes in precipitation had a greater affected on the soil moisture (SM) than the ST at 10 cm depth more (Fig. 4b). The 84 mm
precipitation treatment had significantly lower SM than the 167 mm and 253 mm precipitation treatments, and 420 mm precipitation
had significantly higher SM than the 336 mm and 253 mm precipitation treatments, while SM was not significantly different between
the 167 mm, 253 mm and 336 mm precipitation treatments (Fig. 4b), i.e., a small amount of precipitation variation (increase and
decrease in precipitation) did not change the SM. Throughout the growing season, the soil moisture was lowest in May at 1.13 % and
reached a maximum of 3.22 % in September.
The species importance values (SI) of different families also differed under different precipitation treatments, with Lespedeza
potaninii (Leguminosae), Agropyron mongolicum (Gramineae) and Artemisia scoparia (Asteraceae) being the dominant species in each
treatment area, specifically. 420 mm precipitation treatment had higher SI for Leguminosae than for Asteraceae and Gramineae,
336 mm precipitation treatment had higher SI for Asteraceae than for Gramineae and Leguminosae, and under 253 mm precipitation
(CK), Leguminosae SI were more than those of the Gramineae and Leguminosae (Table 1).
Among the different precipitation treatments, aboveground biomass (AGB) was significantly lower for the 84 mm precipitation
treatment than for the 253 mm precipitation treatment but was not significantly different from the 167 mm precipitation treatment;
AGB was significantly higher for the 420 mm precipitation treatment than for the 336 mm and 253 mm precipitation treatments
(Table 1). For plant aboveground biomass, the effect of the precipitation increases was more positive than that of the precipitation
decreases.

3.2. Seasonal patterns of ecosystem carbon fluxes under a precipitation gradient

In general, the monthly mean net ecosystem carbon exchange (NEE), gross ecosystem photosynthesis (GEP), ecosystem respiration
(ER), soil respiration (SR), and heterotrophic component (Rh) of SR were significantly affected by the precipitation treatments
(P < 0.001, Table 2), except for the autotrophic component (Ra) of SR, which was not significantly affected by the precipitation
treatment (P = 0.759). The carbon flux changes in the desert grassland ecosystem had a clear seasonal pattern (Fig. 5), which behaved
in general agreement with the pattern of precipitation changes during the growing season (Table A.1). Due to the maximum pre­
cipitation in August and September, NEE, GEP, ER and SR all reached their maximum values at the peak of plant growth (August) and
then declined in September with plant senescence, where NEE and GEP showed the same trend and showed a single peak, while ER, SR,
Ra and Rh showed the same trend, and all showed a double peak (Fig. 5).

Table 1
Species importance value (SI) and aboveground biomass (AGB) under different precipitation treatments in August. “0” indicates that there were no
species.
Species 84 mm 167 mm 253 mm 336 mm 420 mm

Lespedeza potaninii 0.260 0.297 0.290 0.164 0.342

Artemisia scoparia 0.234 0.228 0.194 0.309 0.261
Agropyron mongolicum 0.122 0.158 0.244 0.187 0.129
Polygala tenuifolia 0.151 0.052 0.045 0.032 0.041
Salsola collina 0.036 0.109 0.028 0.001 0.036
Scorzoneradivaricata 0.062 0.019 0.031 0.033 0.037
Euphorbia esula 0.004 0.008 0.094 0.004 0.024
Peganum harmala 0.035 0.026 0 0.121 0.037
Cynanchum komarovii 0.086 0 0.021 0.123 0.048
Glycyrrhiza uralensis 0 0.073 0.007 0 0.006
Oxytropis racemosa 0 0.021 0.030 0 0.029
Allium mongolicum 0 0 0.002 0.023 0
Echinops gmelinii 0.011 0 0 0 0.011
Caragana korshinskii 0 0.009 0.013 0 0
Plant aboveground biomass (g m2) 63.44 ± 9.25c 82.23 ± 4.65 bc 104.45 ± 12.21b 111.43 ± 7.2b 141.94 ± 11.45a

Note. Different letters indicate significant differences (P < 0.05) among precipitation treatments.

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Table 2
Repeated-measures ANOVA of precipitation variation and sampling date and their interaction on ecosystem carbon fluxes.
Variance source df F value

NEE ER GEP SR Ra Rh

Precipitation (P) 4 36.42*** 24.59*** 49.21*** 6.17** 0.467 7.20**

Date (D) 4 109.63*** 46.57*** 90.99*** 71.90*** 25.832*** 19.51***
P*D 16 2.27** 2.04* 2.78** 3.36*** 2.13* 2.81**

Note: “*”, P < 0.05; “**”, P < 0.01; “***”, P < 0.001.

Across the growing season (May-September), NEE showed negative values, i.e., net carbon uptake. Specifically, NEE, ER, GEP, and
SR were minimal in May and reached maximum values in July and August, while ER and SR reached maximum values in June and
August (Fig. A.1). In August and September, NEE, ER and GEP were significantly higher under the 420 mm and 336 mm precipitation
treatments than under the 253 mm precipitation treatment (Fig. A.1). Under treatments with reduced precipitation, NEE was
significantly lower in July and August under the 84 mm precipitation treatment than under the 253 mm precipitation treatment, and
ER was significantly lower in August under 84 mm precipitation than under 253 mm precipitation. carbon fluxes did not increase
significantly when precipitation increased in September (late in the growing season) (Fig. A.1).

3.3. Effects of precipitation gradient on ecosystem carbon fluxes

Throughout the growing season, different precipitation treatments significantly affected the seasonal mean NEE, ER and GEP
(Fig. 6a-c). Compared to the 253 mm precipitation treatment (CK), NEE, ER and GEP were significantly increased (P < 0.05) for both
the 336 mm and 420 mm precipitation treatments under the increased precipitation treatment and significantly decreased (P < 0.05)
for both the 84 mm and 167 mm precipitation treatments under the reduced precipitation treatment. The changes in NEE, ER and GEP
due to precipitation treatments are shown (Fig. 6e-g); specifically, the seasonal mean NEE increased significantly by 30 %
(0.89 µmol m− 2 s− 1) and 15 % (0.44 µmol m− 2 s− 1) under 420 mm and 336 mm precipitation, respectively, and by 84 mm and

Fig. 5. Changes in monthly mean values in (a: net ecosystem carbon exchange (NEE), b: ecosystem respiration (ER), c: gross ecosystem photo­
synthesis (GEP), d: soil respiration (SR), and e: heterotrophic respiration (Rh) and f: autotrophic respiration (Ra) of soil respiration).

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167 mm precipitation, respectively, the NEE decreased by 22 % (0. 66 µmol m− 2 s− 1) and 8 % (0.23 µmol m− 2 s− 1) (Fig. 6e). The
seasonal mean ER significantly increased by 58 % (1.72 µmol m− 2 s− 1) and 33 % (0.99 µmol m− 2 s− 1) under 420 mm and 336 mm
precipitation treatments, respectively, while it significantly decreased by 8 % (0.23 µmol m− 2 s− 1) and 4 % (0.11 µmol m− 2 s− 1) under
84 mm and 167 mm precipitation treatments, respectively (Fig. 6f). The seasonal mean GEP significantly increased by 44 %

Fig. 6. Growing season average ecosystem carbon fluxes (a: net ecosystem carbon exchange (NEE), b: ecosystem respiration (ER), c: gross ecosystem
photosynthesis (GEP) and d: soil respiration (SR)) under different precipitation treatments and precipitation variation-induced changes in NEE (e),
ER (f), GEP (g), and SR (h). Different letters indicate significant differences (P < 0.05) among precipitation treatments.

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(2.61 µmol m− 2 s− 1) and 24 % (1.42 µmol m− 2 s− 1) under 420 mm and 336 mm precipitation treatments, respectively, and signifi­
cantly decreased by 15 % (0.9 µmol m− 2 s− 1) and 6 % (0.34 µmol m− 2 s− 1) under 84 mm and 167 mm treatments, respectively
(Fig. 6g). Increasing precipitation had no significant effect on SR, but the seasonal mean SR tended to increase with increasing pre­
cipitation (Fig. 6d). SR reached its maximum (2.23 µmol m− 2 s− 1) under the 420 mm precipitation treatment. The seasonal mean SR
was significantly reduced by 9 % (1.87 µmol m− 2 s− 1) under the 84 mm treatment (Fig. 6h).

3.4. Relationship between ecosystem carbon exchanges and SM, ST and AGB

Monthly mean ecosystem carbon fluxes (NEE, ER, GEP, SR and Ra and Rh components of SR) increased with SM, and the correlation
between monthly mean ecosystem carbon fluxes and SM can be described by a linear functional relationship (Fig. 7a, Fig. A.2). The
response of GEP to SM was more sensitive than ER, as reflected by the slope of the linear functional equation being larger (the slopes of
GEP and ER were 2.47 and 1.33, respectively).
Monthly mean NEE and GEP showed a linear function with soil temperature under precipitation variation and increased signifi­
cantly with ST. There was no significant relationship between ER and SR and ST (P > 0.05) (Fig. 7b).
The carbon fluxes of seasonal ecosystems increase linearly with precipitation and plant aboveground biomass (Fig. 8a-b, Fig. A.3).
Precipitation significantly increased AGB (Table 1), AGB was positively correlated with GEP and ER (the slope of GEP was greater than
that of ER), and precipitation was positively correlated with GEP and ER. Therefore, the increase in GEP may be more attributed to the
increase in aboveground biomass caused by precipitation.
In this experiment, soil and ecosystem respiration were the main factors explaining GEP in addition to moisture, temperature and
biomass. The results of the linear regression model showed that the contributions of GEP to the variability in ecosystem respiration and
soil respiration were 82 % and 79 %, respectively (Fig. 9a-b). SR and ER increased with increasing GEP.

4. Discussion

4.1. Drivers of ecosystem carbon fluxes

In the desert steppe of northern China, the treatment of precipitation and measurement dates and interactions have a significant
impact on the seasonal mean of ecosystem carbon fluxes. In August, plant crown productivity improved due to increased temperature
and enhanced leaf photosynthesis (Niu et al., 2017), and the carbon exchange process was accelerated in an ecosystem where carbon
uptake was dominant. The rate of carbon flux exchange in ecosystems peaks in the middle of the growing season (August) as the plant
growth rate gradually increases (Niu et al., 2008). In September (final growth stage), NEE, ER, and GEP decreased in accordance with
plant aging and decreasing temperature (Fig. 4a, Fig. 5a-c). Similar results were also found in the dry desert grassland (Zhu et al., 2021)
and temperate desert grassland (Niu et al., 2008) of China. In addition, higher carbon exchange was observed in July, August and
September than in May and June in this study. This result implies that the short-term drought due to low rainfall in July had no
significant effect on carbon uptake, which may be related to the water transport effect in desert grassland ecosystems (Niu et al., 2008).
Similar reports have been made in precipitation control experiments of different years (Zhang et al., 2019) as well as in different
ecosystems (Niu et al., 2008). On the one hand, this may be because the plants are still in the early stage of growth (water accu­
mulation) in May and June. When plants generally enter the peak growth stage in July and August, plant biomass increases. Due to the
accumulation of water during the early growth stage, water limitation in the peak growth stage is alleviated. With the increase in
rainfall in August, soil moisture no longer becomes a limiting factor, and at the same time, soil nutrient effectiveness also increases
(Bahn et al., 2009). On the other hand, suitable temperature, moisture conditions and more active plant root activity can simulta­
neously promote ecosystem respiration (Sun, 2017). Although soil respiration also releases large amounts of CO2, the NEE and GEP are
relatively high due to the strong plant growth and photosynthesis during this period, resulting in the strongest carbon uptake activity at
this stage, which is obviously more favorable to the GEP. It has been shown that soil moisture is significantly influenced by changes in

Fig. 7. Relationship between (a) soil moisture (SM) and (b) soil temperature (ST) and net ecosystem C exchange (NEE), gross ecosystem photo­
synthesis (GEP), ecosystem respiration (ER) and soil respiration (SR) in the growing season.

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J. Yu et al. Global Ecology and Conservation 38 (2022) e02202

Fig. 8. Relationship between (a) precipitation and (b) aboveground biomass (AGB) and net ecosystem C exchange (NEE), gross ecosystem
photosynthesis (GEP), ecosystem respiration (ER) and soil respiration (SR)) in the growing season.

Fig. 9. Relationships of gross ecosystem photosynthesis with (a: soil respiration (SR) and b: ecosystem respiration (ER)).

precipitation, while ecosystem respiration varies with soil moisture (Su et al., 2020). Yue et al. (2016) reported in the
precipitation-sensitive horqin sandy land that limited precipitation significantly affected the soil water content in the region.
In this study, the first ER and SR peaks occurred in June with 28.8 mm of rainfall, and the second peak occurred in July August with
23.6 mm of rainfall (2.4 mm in July). The soil moisture first peak in June was due to higher rainfall. For moisture-limited desert
ecosystems, respiration is more sensitive to changes in soil water content (Wang et al., 2019), the average soil temperature in June was
lower (19.5 ◦ C, Fig. 4a), and soil moisture evaporation was weaker. The relative abundance of soil moisture increases the effectiveness
of soil soluble organic matter required for microbial activity, which will provide sufficient substrate for microbial colonization (Wan
et al., 2002), resulting in increased soil respiration (Wang et al., 2019). This is consistent with this study’s conclusion that hetero­
trophic respiration is significantly and positively correlated with SM and precipitation (Fig. A.2, Fig. A.3). The low precipitation in
July, however, with the increase in temperature, intensified evaporation and produced some water stress on plants and microor­
ganisms, which might offset the promotion effect of warming on SR (Niu et al., 2008). In August, the precipitation increased again, and
the temperature also increased (26 ◦ C, Fig. 4a). It has been suggested that larger precipitation directly affects air flow between soil
crevices, increasing leaching of soil organic carbon and limiting the activity and abundance of soil microorganisms, ultimately off­
setting the positive effect of precipitation on ER (Zeppel et al., 2014). In contrast, ecosystem respiration and microbial respiration

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J. Yu et al. Global Ecology and Conservation 38 (2022) e02202

increased with increasing precipitation in this study (Fig. 8a, Fig. A.3), which is not consistent with the above findings and may be
related to precipitation conditions in the arid zone. Respiration reached a second peak in August, possibly because warming may affect
microbial community structure through the antagonistic effect of lower soil moisture and sufficient precipitation, which directly af­
fects microbial respiration (Zhang et al., 2013).
Soil moisture is important environmental determinants of plant processes and soil processes in many terrestrial ecosystems (Melillo
et al., 2002). It has been shown that increased precipitation leads to higher soil moisture (Gherardi and Sala, 2013), and a certain
amount of soil moisture can stimulate the effectiveness of nitrogen fertilizer fertilization (Guo et al., 2018; Sun et al., 2016), thus
leading to increased vegetation productivity and enhanced photosynthetic fixation of plants (Ye et al., 2016). The results of this study
showed that the average soil moisture increased with increasing precipitation from May to September, and the values of NEE, ER, GEP
and SR increased linearly with increasing soil moisture (Fig. 7a). Because NEE and GEP are mainly influenced by plants, the changes in
ER and SR are mainly influenced by carbon availability from the soil carbon pool and microbial activity (Li et al., 2021). Increased
precipitation increases soil moisture, stimulating plant growth and microbial activity in semiarid areas and promoting the transport of
carbon from aboveground plant parts to roots; thus, increasing Ra and Rh, which was also verified by the results of the correlation
analysis (Han et al., 2017) (Fig. A.2). During the growing season, GEP is more sensitive to soil water effectiveness than ER and is
reflected by its different slope when plotting precipitation (Fig. 7a), which is in line with the findings in semiarid temperate grasslands
(Xia et al., 2009) and desert grasslands (Yang et al., 2013). In semiarid grasslands, the root systems of herbaceous plants are usually
distributed in the topsoil layer (Ping et al., 2010). Therefore, the deep soil water recharge of grasses is very limited, and GEP is more
limited by drought than ER (Wang et al., 2016). This is shown by the change in GEP is greater than ER when precipitation decreases
(Fig. 6f-g).
As temperature and moisture are the main limiting factors for plant growth in sandy grasslands in arid and semiarid regions,
changes in precipitation will have profound effects on plant physiological and ecological processes and ecosystem structure and
function by altering soil hydrothermal conditions (Butler et al., 2012), ultimately leading to changes in ecosystem carbon fluxes. The
present study showed that precipitation did not significantly alter soil temperature, which is consistent with the results of simulated
precipitation experiments in semiarid grasslands of northern China (Chen et al., 2009) and semi-arid grasslands of the Loess Plateau
(Su et al., 2020). The variation of soil temperature is closely related to soil moisture, but also to various factors such as radiation
balance, thermodynamic properties of the soil and heat flux of the soil (Zhang et al., 2013). Liu et al. (2015) concluded that differences
in soil moisture conditions in sandy grassland habitats would directly affect the thermodynamic properties of soils, and an increase in
proper soil moisture promotes the heat transfer process of soils, leading to a transient increase in soil temperature. And excessive
precipitation such as rainfall increase 100 % treatment served to reduce soil temperature while favoring increased heat transfer (Zhang
et al., 2013). It has been proposed that the response of ecosystem carbon exchange to temperature may be regulated by the soil’s
moisture status. Su et al. (2020) reported that ecosystem C fluxes increased with increasing temperature. This study showed that NEE
increased with increasing temperature due to the significant relationship between GEP and ST (R2 =0.16, P = 0.043). It is worth noting
that there was no significant relationship between ST and SR in this study (Fig. 7b). Meta-analyses have revealed that increased soil
temperature will promote soil respiration (Rustad et al., 2001). One possible reason is that the effect of elevated ST on SR is envi­
ronmentally relevant, and it depends heavily on the initial conditions, especially SM (Christensen et al., 2004). Studies in the arid and
semiarid grasslands of Inner Mongolia also pointed out that SR had a significant positive correlation with soil water content and
temperature but was mainly determined by soil water content (Kang et al., 2019), which is consistent with the results in this study
–that there was a significant positive correlation between SR and SM but not with ST (Fig. 7a-b), which reflects that soil moisture is an
important factor affecting SR.
Annual or perennial drought-tolerant plants are an important component of plant communities in arid and semiarid grassland
ecosystems (Sun, 2017). In arid ecosystems, the greatest limiting factor affecting plant growth is usually water, and an increase in
effective water usually enhances plant biomass (Wenninger and Inouye, 2008). The accumulation of significant biomass in plant
communities is attributed to the combination of photosynthesis and soil fertility (Bai et al., 2008). Photosynthesis in plants is limited by
water availability; therefore, maintaining a high soil moisture content will promote carbon assimilation and thus increase plant
productivity (Yoneyama et al., 2001). In the present study, increased precipitation significantly increased plant aboveground biomass,
and seasonal means of NEE, GEP, ER, and SR were significantly and positively correlated with AGB (Fig. 8b), and AGB decreased with
decreasing precipitation, implying that the increase in AGB due to the increase in precipitation increases the carbon flux of the desert
steppe ecosystem. SM increases with precipitation gradients (Gherardi and Sala, 2013). As a result, the soil microenvironment is
improved, and the microbial activity is enhanced (Han et al., 2017), ultimately determining the ecosystem carbon fluxes (Guo et al.,
2018). In addition, our results show that seasonal GEP is more dependent on aboveground biomass than ER, implying that when
precipitation increases, desert grassland ecosystems become carbon sinks due to the positive response of biomass. Therefore, the effect
of precipitation on carbon flux is not only related to the SM factor (Su et al., 2020) but also to the plant species composition and
productivity (Zhang et al., 2019). In addition, in this study, we found that the perennial herbs Agropyron mongolicum (Gramineae) and
Lespedeza potaninii (Leguminosae) (Zhao et al., 2018; Huang et al., 2018), which grow in arid and low rainfall areas, were distributed in
both 84 mm and 167 mm precipitation treatment sample plots. Rainfall in July September accounts for 60–80 % of the annual rainfall
in the study area (Fig. 1). Therefore, we believe that the growth of the two plant species will not be significantly affected under future
precipitation changes.

4.2. Precipitation gradient effects

Global climate change factors such as precipitation may differentially affect carbon fluxes as well as respiration changes (Chen

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J. Yu et al. Global Ecology and Conservation 38 (2022) e02202

et al., 2009; Su et al., 2020). Our results show that precipitation changes significantly affect NEE, ER, GEP, and SR, which is consistent
with the positive response to increased precipitation reported in most previous semiarid grassland studies (Han et al., 2017; Li et al.,
2017; Zhang et al., 2019). The seasonal means of NEE, ER, GEP, and SR in this study were − 3.09 µmol m− 2 s− 1, 3.43 μmol m− 2 s− 1,
6.52 μmol m− 2 s− 1, and 2.06 μmol m− 2 s− 1, respectively, and NEE, ER, and GEP were similar to those reported previously for this study
area (Zhu et al., 2021) and for the northern temperate grassland (Xia et al., 2009) and loess plateau areas (Su et al., 2020). The
fluctuation range of SR was 1.87–2.23 μmol m− 2 s− 1, which was similar to the results of a desert grassland study (Wang et al., 2019).
The fluctuation range of GEP is 5.06–8.75 μmol m− 2 s− 1, while that of ER is 2.72–4.67 μmol m− 2 s− 1, indicating that GEP is more
influenced by precipitation changes than ER (Tagesson et al., 2016).
In the present study, NEE, ER and GEP increased with precipitation. The increase in precipitation promoted the growth of plant
canopy, which created better conditions for photosynthesis, leading to an increase in GEP and NEE (Ye et al., 2016). The increase in ER
was greater than that of GEP under the precipitation increase treatment because the precipitation increased the SM and stimulated the
soil microorganisms to make ER exceed GEP when the desert grassland ecosystem was used as a carbon source. At the same time,
herbaceous plants respond to the increase in SM and begin to grow, and when GEP exceeds ER, gross ecosystem photosynthesis will
increase with AGB (Fig. 8b), making the desert grassland ecosystem a carbon sink. The decrease in GEP due to precipitation change
exceeds the change in ER (Fig. 6f-g), which is detrimental to carbon sink, and similar situation has been reported in semiarid grasslands
(Li et al., 2017; Niu et al., 2008), and they also demonstrated the criticality of moisture in this process. Soil respiration and precip­
itation both increased and decreased together. Soil respiration requires organic carbon to provide raw materials, and precipitation can
directly affect plant growth and carbon allocation to the root system; therefore, changes in precipitation determine the trend of SR
(Manzoni et al., 2012). In addition, we found that the response of soil respiration to the decreased precipitation treatment was stronger
than the response to the increase precipitation treatment, due to the more pronounced inhibition of plant growth and microbial activity
by decreased precipitation (Wang et al., 2019). The results of the present study also reflected that plant aboveground biomass was
significantly lowest under 84 mm precipitation conditions. There was a significant positive correlation between AGB and SR (R2
=0.87, P = 0.020); as a result, soil respiration was reduced.

4.3. Dependence of respiration on ecosystem photosynthesis

In addition to environmental factors, plant canopy photosynthesis is also influenced by SR and ER (Fig. 9). Since the magnitude of
soil respiration depends on the material basis of respiration and environmental conditions, and the products of photosynthesis in the
aboveground parts of plants are a source of energy and material for the root system and soil microorganisms (Smith et al., 2014). As a
result, GEP can have a driving effect on soil respiration (Wertin et al., 2016). The present study also demonstrated the positive
dependence of soil respiration on gross ecosystem photosynthesis (Fig. 8). In addition, Ma et al. (2020) reported a strong regulation of
soil respiration by photosynthesis in the Gurbantunggut Desert, but the process was significantly correlated with soil water content.
The enhanced soil water availability with increased precipitation will help provide more access to obtain the substrates for soil mi­
crobial respiration (Manzoni et al., 2012), especially in arid ecosystems. However, in this study, although increased precipitation
(420 mm) caused an increase in soil moisture, our study showed that the precipitation treatment did not significantly alter the
relationship between above- and below-ground carbon fluxes, with a strong coupling between the two under different precipitation
treatments (Fig. A.4). A temperature manipulation experiment in a dryland community also showed that although changes in soil
moisture due to warming reduced plant photosynthesis and soil carbon fluxes, it did not change the coupling relationship between
them (Wertin et al., 2016). Nord et al. (2015) suggested that soil type may be the primary cause of the coupled relationship between
plant photosynthesis and soil respiration, and that for many of the most common soil types changes in photosynthesis do not
necessarily affect soil respiration. The slope of ER versus GEP (0.52) in this study indicates that an average increase of 1 μmol m− 2 s− 1
in GEP is associated with an increase of 0.52 μmol m− 2 s− 1 in ER, suggesting that photosynthetic products accumulated during carbon
sequestration by plants have a significant impact on ER (Wang et al., 2016). This indicates that a strong coupling between above- and
belowground fluxes in desert grassland ecosystems (Wertin et al., 2016). Similar studies have been reported in African arid grasslands
(Tagesson et al., 2016) and in temperate heath (Larsen et al., 2007), oak/grass savannas (Ma et al., 2007) and degraded grasslands (Du
and Liu, 2013).

5. Conclusions

We conclude that the seasonal dynamics of NEE and GEP exhibited a single peak, whereas ER and SR exhibited a bimodal peak
across all precipitation treatments. Changes in precipitation significantly affected ecosystem carbon fluxes, with decreased precipi­
tation suppressing GEP and thus reducing NEE, however, decreased precipitation had no effect on ER. Increased precipitation has a
greater effect on GEP than ER, leading to a carbon sink. In addition, abiotic factors, such as soil temperature and moisture, as well as
biotic factors, such as plant aboveground biomass, are important in regulating ecosystem carbon fluxes in semiarid desert steppe. NEE
and GEP increased with increasing ST, SM and AGB, and GEP was more sensitive to SM than ER. Precipitation did not change the
coupling between above- and below-ground fluxes, but the strong dependence of respiration on total ecosystem photosynthesis will
affect above- and below-ground carbon cycling processes in semiarid desert steppes. Used together, as water effectiveness increases,
GEP increases more than ER, resulting in enhanced NEE. The incorporation of biotic and abiotic factors for the scientific management
of desert steppes in a future climatic context of increased precipitation will ultimately give the desert steppes of northern China the
potential to become a large carbon sink.

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Funding

This study was supported by the National Natural Science Foundation of China, China (32160336); Ningxia Key Research and
Development Program Project, China (2020BEG03046); and Ningxia University First-class Discipline Construction Project of Grass
Science, China (NXYLXK2017A01).

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to
influence the work reported in this paper.

Appendix A. Supporting information

Supplementary data associated with this article can be found in the online version at doi:10.1016/j.gecco.2022.e02202.

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