Yu Wu , Hai Zhou , Xin-Jun Zheng , Yan Li 1* and Li-Song ... changes in the water use...Knapp, 1995; Tian et al ... Previous studies suggested that the isotopic ... all samples were

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Seasonal changes in the water use strategies of three co-occurring desert shrubs Yu Wu1,2, Hai Zhou1,2, Xin-Jun Zheng1, Yan Li1* and Li-Song Tang1

1 State Key Lab of Oasis and Desert Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, Xinjiang, China 2 University of Chinese Academy of Sciences, Beijing, China Corresponding author: Dr. Yan Li E-mail: [email protected] Tel: +86 991 7885415 Fax: +86 991 7885320

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Abstract

Water is a major limiting factor in desert ecosystems. In order to learn how plants cope with changes in water resources over time and space, it is important to understand plant-water relations in desert region. Using the oxygen isotopic tracing method, our study clarified the seasonal changes in the water use strategies of three co-occurring desert shrubs. During the 2012 growing season, δ18O values were measured for xylem sap, the soil water in different soil layers between 0 and 300 cm depth and groundwater. Based on the similarities in δ18O values for the soil water in each layer, three potential water sources were identified: shallow soil water, middle soil water and deep soil water. Then we calculated the percentage utilization of potential water sources by each species in each season using the linear mixing model. The results showed that the δ18O values of the three species showed a clear seasonal pattern. Reaumuria songarica used shallow soil water when shallow layer was relatively wet in spring, but mostly took up middle soil water in summer and autumn. Nitraria tangutorum mainly utilized shallow and middle soil water in spring, but mostly absorbed deep soil water in summer and autumn. Tamarix ramosissima utilized the three water sources evenly in spring and primarily relied on deep soil water in summer and autumn. R. songarica and N. tangutorum responded quickly to large rainfall pulses during droughts. Differential root systems of the three species resulted in different seasonal water use strategies when the three competed for water. KEY WORDS seasonal change; water use strategies; water resource; co-occurring desert shrubs; northwest China


Introduction

Water determines a great many ecosystem processes in arid and semiarid regions, such as carbon storage, species survivorship, competition and primary production (Briggs and Knapp, 1995; Tian et al., 1999; Fay et al., 2003; Bunker et al., 2005). As the main water input in desert ecosystems (Noy-Meir, 1973), precipitation dominates water availability or water resources for plants. However, due to the uneven distribution of precipitation (Loik et al., 2004), soil moisture in arid ecosystems is extremely variable both in space and time (Schwinning and Ehleringer, 2001). There are prevalent periodic or chronic water deficits for some desert plants. To survive and meet metabolism or growth requirements, perennial plants must regulate their water use and their roots have to acquire the remaining soil moisture through extended drought periods (Ehleringer et al., 1991; Dawson, 1993). Therefore, precipitation seasonality influences the water use patterns of dominant species as well as the composition and structure of plant communities.

It has been suggested that the exploitation of spatially and/or temporally distinct zones of soil moisture by plants allows the coexistence of different life-forms (Noy-Meir, 1973). For example, most grasses are opportunistic, utilizing the short-term availability of water in the upper soil layers, while shrubs rely on a deeper soil water resource that is more stable over the long term (Soriano and Sala, 1983). This concept coincided with the vertical distribution of roots in different plants (Dodd et al., 1998). But root presence per se may not be a reliable indicator of actual water uptake dynamics (Ehleringer and Dawson, 1992), which is dependent on root activity in soil areas where moisture is available (Donovan and Ehleringer, 1994), especially over short time scales (e.g. a season). For some plants, the water source may change with the growth stage or with the water availability over different seasons. During establishment, small streamside trees depend on stream water in the upper layers. Once established, mature individuals use a deeper water source (Dawson and Ehleringer, 1991). In the dry season, Banksia prionotes derives the majority of the water it needs from deeper sources; while in the wet season, most of the water is derived from shallower sources (Dawson and Pate, 1996). The water use pattern of Juniperus ashei in Edwards Plateau of USA exhibited a similar switch in water sources (McCole and Stern, 2007). Therefore, explorations of seasonal water use strategies by different plants are necessary in order to improve understanding of plant-water relations and water balances in these ecosystems.

Stable isotope methods offer effective means of identifying water sources utilized by plants (Flanagan et al., 1992; Schwinning et al., 2005; Duan et al., 2008; Liu et al., 2010). Previous studies suggested that the isotopic fractionation of water occurs during phase transitions, but not during advective flow of water (Dawson and Ehleringer, 1991; Ehleringer and Dawson, 1992; Dodd et al., 1998; Dawson et al., 2002). There is no isotopic fractionation during water uptake by roots and transport from root to shoot while isotopic fractionation indeed occurs in leaves during transpiration (Dawson and Ehleringer, 1991; Ehleringer and Dawson, 1992; Dawson et al., 2002). Coupled with the seasonal variation in the isotopic characteristics of precipitation (Dansgaard, 1964), the natural composition of hydrogen and oxygen isotopes in different water sources provides a non-artificial label for plant water sources. Thus, the isotopic composition of xylem water is a mixture of different water sources, reflecting the various zone(s) and depth(s) from which the plant is currently


extracting soil water (Ehleringer and Dawson, 1992). By comparing and analyzing the isotopic characteristics of xylem waters and those of potential water sources (e.g. rain water, soil water and groundwater), a linear mixing model could be used to calculate the percentage use of each potential water source by plants (White et al., 1985; Phillips and Gregg, 2003; Phillips et al., 2005).

Although the perennial woody life form is often distinguished as a group for comparison with other life forms, there is a great deal of variation within shrubs with regards to seasonal water stress and rooting depth and distribution (Donovan and Ehleringer, 1994). Tamarix ramosissima, Nitraria tangutorum and Reaumuria songarica are co-occurring dominant shrubs in the Junggar basin, northwest China. Previous studies have focused on the physiological response of their twigs to rainfall (Xu and Li, 2006; Li, 2010). The rooting patterns of the three shrubs have also been investigated to elucidate the water use strategies during drought periods (Sun and Yu, 1992; Xu and Li, 2009). However, the dynamics of water use by roots throughout an entire growing season remain largely unexplored. The objective of our research was to investigate the seasonal changes in the source water used by these co-occurring shrubs that have different root systems in a desert habitat. Materials and Methods Site and species description

The study was conducted at Fukang Station of Desert Ecology, Chinese Academy of Sciences, located on the southeast edge of Gurbantunggut Desert (44°17′N, 87°56′E, 475 m a.s.l.). It has a typically temperate continental arid climate and in the hot dry summer, the highest temperature is above 35°C, but during the winter, the average snow depth is 20~30 cm, with stable snow cover lasting for 100~150 d (Zhou et al., 2009). The annual mean temperature is 6.6°C and the annual mean precipitation is about 160 mm. The soil type at this site is silty clay-loam with a high salinity and the upper 1 m of soil is extremely dry due to the high pan-evaporation (about 2000 mm per year). The groundwater table depth is about 5 m.

The profiles of three co-occurring shrubs are shown in Table 1. Previous excavations in this area revealed that the tap root of N. tangutorum was no more than 2 m in depth. The absorbing root area of N. tangutorum was recorded by Sun and Yu (1992). Root information for T. ramosissima and R. songarica was reported by Xu and Li (2009) who conducted experiments in the same habitat. Sample collection

From March to October of 2012, suberized twigs (diameter 0.3~0.5 cm, length 3~5 cm) from the plants were sampled at half-monthly intervals for xylem water. For each species, four replicate samples were cut from four individuals. We decorticated twigs gently and quickly when they were cut. To prevent changes in the isotopic values through evaporation, all samples were immediately placed into screw-cap glass vials sealed by parafilm and stored in a freezer prior to water extraction and isotopic analysis. The first samples were taken on day of year (DOY) 88, and the last sampling was on DOY 291.

The soil samples were collected using a hand auger that soil cores were taken next to the sampled plants on the same days as the plants were sampled (also at half-monthly intervals).


The total depth augered was 0~300 cm. Soil samples between 0 and 100 cm were obtained at 10 cm intervals and those between 100 and 300 cm were obtained at 20 cm intervals. Four replicates for each layer were sampled from four independent cores. Then soil samples were divided into two parts: one was sealed in glass vials and frozen until they were needed for isotopic analysis of soil water and the other was sealed in soil tins for subsequent measurement on gravimetric soil water content (SWC, %), which were obtained with the oven-drying method.

Groundwater samples were collected from a nearby well every month and were sealed and stored at 2°C. We collected rainwater from twelve precipitation events. Precipitation samples were collected from standard rain gauge immediately after each individual rainfall event and were filtered using a 0.22 μm filter. Each sample was pipetted into a small vial sealed by parafilm and refrigerated at 2°C until isotope analysis. Precipitations and temperatures were recorded by a weather station near the site.

In addition, to investigate the responses of the water use patterns to the rainfall pulses in different seasons, we tracked natural rainfall events. Plant twigs were sampled on 1, 2, 3, 5, 8 days after 5.6 mm spring rainfall (on DOY 141) and 7 mm autumn rainfall (on DOY 266), respectively. Likewise, when an 11.9 mm summer rainfall occurred on DOY 216, we sampled plant twigs on the same day (0), and then sampled again 1, 2, 4, 7 and 17 days after the precipitation event. Meanwhile, in order to obtain the soil water content and isotopic values of the soil water within the 0~100 cm layer, four soil sample replicates were collected at 10 cm intervals near the sampled plants. All samples were immediately stored in glass vials and were kept frozen until needed for isotopic analysis. Analyses and calculation

Hydrogen isotope fractionation has been observed during water uptake in some xerophytes (Ellsworth and Williams, 2007). Therefore, we chose 18O as a tracer. Xylem water and soil water were extracted using a cryogenic vacuum distillation extraction line and the extracted water was stored in sealed glass vials at 2°C. Then the oxygen isotopic composition of the water was determined by a liquid water isotope analyzer (LWIA, DLT-100, Los Gatos Research Inc., Mountain View, CA, USA). The oxygen isotopic composition can be expressed as:

δ18O = (Rsample / Rstandard –1) × 1000‰ where RSample and RStandard are the oxygen stable isotopic composition (18O/16O molar

ratio) of the sample and the standard water (Standard Mean Ocean Water, SMOW), respectively. To eliminate the effect of methanol and ethanol contamination, δ18O values for the xylem water were corrected by a standard curve. Creation of standard curves

The standard curves were created by engineers from Los Gatos followed Schultz et al. (2011). The procedures were as follows:

Deionized water (DI) (simplicity UV, Millipore Inc., Milford, MA, USA) were spiked with varying concentration methanol or ethanol (99.9% chromatographic pure). Concentration gradient for methanol (μL·L-1): 0, 10, 20, 30, 40, 60, 80, 100, 120, 140, 160, 200, 240, 280, 320, 350, 380, 400, 420, 450, 480, 500, 520, 550, 580, 600, 620, 640, 660,


680, 700, 720, 740, 760, 780 and 800. Concentration gradient for ethanol (mL·L-1): 0, 2, 6, 10, 15, 20, 25, 30, 35 and 40. Three repetitions were done for each concentration.

The δ18O values of above solution were measured by an isotope ratio infrared

spectroscopy (IRIS) analyzer — the Liquid Water Isotope Analyzer. With the Spectral

Contamination Identifier (LWIA-SCI), a post-processing software, narrow-band metric (NB) represented methanol contamination, and broad-band metric (BB) represented ethanol contamination. The Relationships between NB, BB and the offsets of δ18O values were obtained: ∆δ18O(y) ~ lnNB(x): y = 0.1455 x2 + 0.0255x + 0.329, R2 = 0.9946 (Figure 1a) ∆δ18O(y) ~ BB(x): y = -9.1411x + 9.1269, R2 = 0.8962 (Figure 1b)

The methanol resulted in more positive isotope values, and the offsets should be subtracted from the original isotope values. The ethanol resulted in more negative δ18O values, and the offsets should be added to the original δ18O values. The main contaminant in our samples was methanol which is within the range of 10~280 μL·L-1. Comparison between IRIS and IRMS

The δ18O values from IRIS analysis were compared with corresponding data obtained from an Isotope Ratio Mass Spectrometry (IRMS) (Finnigan MAT 253, Thermo finnigan, Bremen, Germany). The xylem water of T. ramosissima, N. tangutorum, R. songarica was extracted by cryogenic vacuum distillation. There were 12 samples for each species. All samples were filtered by 0.22 μm filter. Each sample was divided into two sub-samples and δ18O values were measured by IRIS and IRMS, respectively. IRIS data (before and after correction) were compared with IRMS data in Figure 2. Without correction, the absolute value of mean difference in δ18O between IRIS data and IRMS data was (1.95 ± 0.22)‰. After correction, the absolute value of mean difference in δ18O between IRIS data and IRMS data was (0.47 ± 0.03)‰. Overall, the corrections effectively eliminated the discrepancies in δ18O values between IRIS and IRMS method.

To calculate the amounts of the different water sources used by each species at each sampling time, the isotopic values for the xylem water were compared with those of potential water sources using the IsoSource model (Phillips and Gregg, 2003). Potential water sources were the soil waters within the different layers that had been collected on the same day as the plants were sampled. Three potential water sources were used in our research (see below), source increment was defined as 1% and mass balance tolerance was defined as 0.1‰. First, we obtained the percentage utilization of the different water sources by each species on each sampling day and then calculated the mean and the possible range of water utilization in each season. Due to its root limitation, R. songarica could not access the deep water source directly, so we quantified the percentage utilization of the shallow and middle soil water sources by R. songarica using a two-compartment linear mixing model (White et al., 1985). For the rain pulses study, data input to the IsoSource model have two origins: 0~100 cm δ18O values of soil water and xylem water were sampled on the day of concern, while the δ18O values of 100~300 cm were taken as the nearest monitored values, which were obtained at half-monthly intervals. During the experimental period, the soil water content and the δ18O


values of soil water below 100 cm were almost unaffected by a single rainfall pulse (see Figure 5). Data analysis

Multiple comparison of δ18O values for the soil water from all individual layers and the groundwater were processed by Fisher’s least significant difference method (LSD) in the one-way ANOVA (seasonal changes) module in SPSS 13.0. The significance level was P < 0.05.

Based on the similarities in δ18O values for the soil water in each layer, we divided the soil profile into three major sections (0~50 cm, 50~180 cm and 180~300 cm). Accordingly, three potential water sources were identified as follows: (1) shallow soil water (0~50 cm), δ18O values varied significantly with season and depth; (2) middle soil water (50~180 cm), δ18O values decreased with depth, but showed no apparent seasonal changes and (3) deep soil water (180~300 cm), δ18O values were relatively stable, were very similar to those of the groundwater and showed no significant variations for depth and season. Results δ18O values for rain water and precipitation amount

The average oxygen isotope ratios (δ18O) of rain water and individual rainfall amount from February to October of 2012 are shown in Figure 3. The δ18O values for rain water varied considerably among events, ranging between -22.8‰ and 1.7‰, and showed significant seasonal variation. Due to the temperature effect (Dansgaard, 1964), the δ18O values for rain water were lower in spring (March~May) and autumn (September~October) and higher in summer (June~August) (Figure 3).

In our study region, the total rainfall from February to October 2012 was 94.6 mm. Most events were less than 5 mm, especially in summer, and 68% of rainfall frequency was less than 1 mm. The largest event was 11.9 mm, which occurred on DOY 216.

δ18O values for soil water and soil water content

The δ18O values for soil water and soil water content (SWC) in each layer in the 0~300 cm soil profile are displayed in Figure 4. Surface soil waters have highly variable δ18O values due to inputs from rains with variable δ18O signatures and evaporative enrichment. The Fisher’s multiple comparison found that in the upper 50 cm layers, the δ18O values for soil waters were significantly higher in summer and autumn than in spring (P < 0.018, Figure 4a), and dramatically dropped as the depth increased. The δ18O values for soil waters below 50 cm showed no apparent seasonal variation (0.09 < P < 0.885), and progressively declined with increasing depth. Groundwater had constant δ18O values, at -11.7 ± 0.1‰ (mean ± SE), over the whole growing season. In addition, the δ18O values of soil waters from 180 to 300 cm were indistinguishable from that of groundwater (0.057 < P < 0.767 for spring; 0.126 < P < 0.838 for summer and 0.444 < P < 0.979 for autumn).

Although there were subtle differences in SWC between the seasons, the general trend for SWC was similar at three seasons (Figure 4b). In the top 50 cm of the soil profile, SWC fluctuated with the seasons. The SWC at 0~20 cm depth was higher in spring, but was less


than 5% in the summer and autumn (Figure 4b). In the middle part of the soil profile, SWC increased slightly with depth. Between 180 and 300 cm, SWC exhibited no obviously seasonal changes, but increased sharply from 8% at 180 cm depth, peaked at 23% at 220 cm depth and then decreased steadily.

The responses of 0~100 cm SWC and δ18O values of soil water to rainfall pulses are shown in Figure 5. Both SWC and δ18O values of soil water within 0~10 cm layer were significantly affected by rainfall pulses and evaporation. However, those within 10~50 cm were only marginally affected and those of 50~100 cm were almost uninfluenced. Seasonal changes in the δ18O values of xylem water

Figure 6 shows the seasonal changes in δ18O values of xylem water for the three shrubs. All the δ18O values for R. songarica were higher than those of the other two, except in the early spring and in the last data sets. The average δ18O values for R. songarica, N. tangutorum and T. ramosissima were –6.8 ± 0.5‰, –9.5 ± 0.4‰ and –10.5 ± 0.4‰, respectively (Figure 6, P < 0.001, n = 14).

The δ18O values for xylem water within R. songarica showed a clearly seasonal variation. In spring, late summer and early autumn, δ18O values were close to that of rain water, but they significantly dropped between mid-June and mid-July (Figure 6). N. tangutorum showed a very similar pattern, with δ18O value fluctuations declining when entering summer. It should be noted that between mid-June and early August, δ18O values for N. tangutorum coincided with those for T. ramosissima and were very similar to that of groundwater (Figure 6). For T. ramosissima, the δ18O values ranged between –11.6 ± 0.1‰ and –6.6 ± 0.4‰. When entering summer, the δ18O values continuously declined (became more negative). Over the course of the whole summer to early autumn, the xylem water in T. ramosissima had fairly stable δ18O values, which were similar to that of groundwater (Figure 6). Seasonal changes in water use strategies among the three shrubs

For T. ramosissima, the contributions made by the three sources were relatively equal in spring, and the ranges were 0~81%, 0~82% and 0~73% for shallow, middle and deep soil water, respectively. Thereafter, T. ramosissima exploited the deeper water sources. In summer, the deep soil water accounted for 74~100% (Figure 7a). In autumn, the utilization of middle soil water increased slightly, but that of deep soil water was still up to 43~99% (Figure 7a).

During the experimental period, the contribution of middle soil water for N. tangutorum could not be adequately resolved using stable isotope with possible contributions ranging from 0 to 100% (0~97% in spring and summer, 0~100% in autumn) (Figure 7b). The relative contribution of shallow soil water varied in wide ranges in spring (0~78%), but not wide in summer and autumn (Figure 7b). The contribution of deep soil water varied in a narrow range in spring, but then ranges became considerably wide in summer (0~99%) and autumn (0~87%) (Figure 7b).

In spring, the contribution of shallow and middle soil water was nearly equal (approximately 50% from each layer respectively) for R. songarica (Figure 7c). While in summer and autumn, R. songarica mainly derived water from middle soil water (>75%), with less water from shallow soil (Figure 7c).


Variations in water use patterns after rainfall pulses

To further investigate the effects of a rainfall pulse on the water use patterns of the three shrubs, we traced the changes in δ18O values of xylem water for 17 days after a natural, large event in summer. For T. ramosissima, the contribution of the deep soil water was almost up to 100%, and the contribution from shallow or middle soil were negligible both before and after rainfall (Figure 8a). This indicated that T. ramosissima did not use rain water in the shallow or middle soil layers. In contrast, N. tangutorum showed a quick response to the rain pulse. On the 2nd day after rainfall, the percentage of shallow and middle soil water increased from nearly zero to 0~29% and 0~95%, respectively. Meanwhile, the contribution percentage of deep soil water decreased from 90~98% to 5~72% (Figure 8b). R. songarica responded even quicker to this precipitation. On the 1st day after rainfall, the contribution by shallow soil water immediately increased from 31.2 ± 4.3% to 71.5 ± 5.6%. Thereafter, the proportion of shallow soil water gradually declined, whereas that of middle soil water gradually increased (Figure 8c). For the 5.6 mm spring rainfall, the three species did not response significantly (Figure 9). For the 7 mm autumn rainfall pulse, the responses of T. ramosissima and R. songarica were similar with those to the summer rainfall pulse (Figure 10a and c), while the contribution range of middle soil water by N. tangutorum was not stable as it did in summer pulse (Figure 10b). Discussion

The plant root system type is fundamental in determining the water-use strategy of desert shrubs and the physiological responses of a plant to an occasional rainfall pulse (Xu and Li, 2006). This study demonstrated the water use strategies among deep and shallow-rooted shrubs (Xu and Li, 2006). In the current study, we focused on the water use dynamics over the different seasons and following large rainfall pulses and have shown how co-occurring shrubs are well-adapted to utilizing different water sources in a desert environment. Root distributions and water use strategies by the three shrubs

Previous excavation studies showed that the vertical distribution of root systems of the three species differed significantly. For T. ramosissima, 70% of the total absorbing roots occurred in the 200~310 cm soil layer, but the 0~60 cm soil layer contained less than 5% of the roots (Figure 11a). The absorbing root area of N. tangutorum in each soil layer has not been investigated yet, and we failed to collect details of that from published literatures. Based on our knowledge, N. tangutorum has a dimorphic root system with horizontal roots extending to 4~6 m and a tap root of which could reach 2 m. However, more than 2/3 of total root area was restricted to the top 40 cm of the soil profile (Sun and Yu, 1992). For R. songarica, the root depth was less than 1 m, with more than 90% of total absorbing root area occurring between 0 and 60 cm (Figure 11b).

The marked differences in rooting patterns among the three shrubs resulted in the spatial separation of water acquisition in this desert community. Shallow-rooted R. songarica showed great ability in exploiting water available in shallow and middle soil layers (Figure 7c)


and were more sensitive to the rainfall pulses during drought (Figure 8c and 10c). However, the high percentage utilization of shallow soil water derived from rainfall could not be maintained by R. songarica and the fraction made up by middle soil water rose quickly following infiltration (Figure 8c and 10c).

Due to its dimorphic rooting habit, N. tangutorum was able to flexibly shift between possible water sources. In summer, N. tangutorum used deep soil water as its major water source (Figure 7b), but following the large rain event, it responded rapidly by taking up more shallow and middle soil waters (Figure 8b). This is probably due to a trade-off between the activity of shallow and deep roots (Williams and Ehleringer, 2000). It may not be advantageous for perennials to maintain active roots in upper soil layers over the whole summer (Ehleringer and Dawson, 1992), but it is beneficial to develop new feeding roots or activate surface root activities after a large rainfall event (Dawson and Pate, 1996).

Because the antecedent soil water conditions were fine in spring (Figure 5a), the three species did not show markedly responses to the spring rainfall pulse (Figure 9). In summer and autumn, 0~10 cm SWC peaked on the 1st day after rainfall events (Figure 5c and e), and the amounts of the shallow soil water utilization by R. songarica and N. tangutorum reached their highest values on day 1 or 2 after rainfall (Figure 8b and c, Figure 10b and c). This was similar to the dominant species in the Ordos Plateau of northwestern China (Cheng et al., 2006). The 50~100 cm SWC did not significantly increase after rainfall pulses (Figure 5c and e). This indicated that the water use from this layer likely did not change either, although the possible ranges of middle soil water used by N. tangutorum were highly varying as given by IsoSource (Figure 8b, Figure 10b). The xylem water (the water use by the plant) was likely a mixture of deep soil water (the source before the rain) and surface water which was significantly increased after rain (Figure 5c and e). Namely, water use dynamics was determined by root activity rather than root presence.

Comparatively, although the roots of T. ramosissima were distributed continuously throughout the soil profile, it seemed that the most active sites for water absorption were limited to the deeper soil layers. This may be because the shallow water is not a reliable water source for T. ramosissima, while deep soil water, which is derived from groundwater, represents a stable water source. When the deep water source was utilized, the variable shallow soil water was left almost unexploited by T. ramosissima in the drought period (Figure 7a). Thus T. ramosissima did not take up any pulse water, even after the large rain event during summer (Figure 8a). These results implied that the shallow water source may be of limited importance to the long-term water balance of T. ramosissima. In addition, the water use patterns of T. ramosissima and R. songarica fit well with previous research on the physiological responses of their twigs to rainfall (Xu and Li, 2006). Transpiration, leaf water potential and water-use efficiency in T. ramosissima were stable during the drought period, while R. songarica responded strongly to rain pulses, in terms of leaf water potential and transpiration.

Seasonal competition for water among the three co-occurring shrubs

It is well documented that competition for water in deserts influences species interactions and community dynamics (Fowler, 1986). The different types of rooting patterns among species may be adaptations for minimizing competition for water during prolonged


drought conditions (Dawson and Pate, 1996). The three shrubs exhibited seasonal inter-specific competition for water. At the

beginning and end of the growing season, the three species tended to compete for middle soil water. On the first and last sampling day, δ18O values for the three species were very similar (for the first sampling, –8.1 ± 0.4‰, P = 0.335 and for the last sampling, –9.6 ± 0.1‰, P = 0.967, Figure 6) to those of the corresponding middle soil water values. This was probably due to snow water recharging in spring (Zhou et al., 2009) and continuous medium rains infiltrating the soil in autumn (Figure 3), resulting in large amounts of soil water being stored in the middle layers during these two seasons. In the dry summer, with declining water availability in the shallow and middle soil layers, both N. tangutorum and T. ramosissima competed for the deep water source (Figure 7a and b). Their δ18O values coincided for a long time and were similar to that of the groundwater (Figure 6). The deep water source was beyond the reach of R. songarica, and the high soil temperatures (Ma et al., 2012) may have inhibited its surface root activity (Williams and Ehleringer, 2000). Therefore, R. songarica mainly utilized the middle soil water during summer (Figure 7c).

The difference in the capacity to use rainfall pulses among the three dominant species might greatly influence the composition and structure of the community. The different sized rainfall events infiltrated different soil layers. Small rainfall events usually recharge the shallow soil water, whereas large events can infiltrate deeper layers. Thus, altered precipitation regimes over long periods determine surface versus deep layer water availability for plants that co-exist with each other. Based on the possible changes in local precipitation patterns, we predict that under fixed rainfall amounts, frequently occurring small events would favor an increase in R. songarica and N. tangutorum, while occasionally large events will promote T. ramosissima, and will benefit N. tangutorum. From the long term perspective, the highly opportunistic water-use strategy by N. tangutorum could be put at an advantage when competition for water occurs within the ecosystem. Acknowledgements This research was supported by a grant to Li-Song Tang from the Natural Science Foundation of China (No. 41171049), a cooperative China-New Zealand research project (No. 2011DFA31070) and the ‘Western Light’ program of the Chinese Academy of Science (No. XBBS201001). We thank all the staff at the Fukang Station of Desert Ecology for their help in the laboratory analysis and field sampling. And we thank Jie Ma and Jiang-bo Xie for reading and improving the manuscript.


References Briggs JM, Knapp AK. 1995. Interannual variability in primary production in tallgrass prairie:

climate, soil moisture, topographic position, and fire as determinants of aboveground biomass. American Journal of Botany 82: 1024–1030.

Bunker DE, DeClerck F, Bradford JC, Colwell RK, Perfecto I, Phillips OL, Sankaran M, Naeem S. 2005. Species loss and aboveground carbon storage in a tropical forest. Science 310: 1029–1031.

Cheng XL, An SQ, Li B, Chen JQ, Lin GH, Liu YH, Luo YQ, Liu SR. 2006. Summer rain pulse size and rainwater uptake by three dominant desert plants in a desertified grassland ecosystem in northwestern China. Plant Ecology 184: 1–12.

Dansgaard W. 1964. Stable isotopes in precipitation. Tellus 16: 436–468. Dawson TE. 1993. Hydraulic lift and water use by plants: implications for water balance,

performance and plant-plant interactions. Oecologia 95: 565–574. Dawson TE, Ehleringer JR. 1991. Streamside trees that do not use stream water. Nature 350:

335–337. Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP. 2002. Stable isotopes in plant

ecology. Annual Review of Ecology and Systematics 33: 507–559. Dawson TE, Pate JS. 1996. Seasonal water uptake and movement in root systems of

Australian phraeatophytic plants of dimorphic root morphology: a stable isotope investigation. Oecologia 107: 13–20.

Dodd MB, Lauenroth WK, Welker JM. 1998. Differential water resource use by herbaceous and woody plant life-forms in a shortgrass steppe community. Oecologia 117: 504–512.

Donovan LA, Ehleringer JR. 1994. Water Stress and Use of Summer Precipitation in a Great Basin Shrub Community. Functional Ecology 8: 289–297.

Duan DY, Ouyang H, Song MH, Hu QW. 2008. Water Sources of Dominant Species in Three Alpine Ecosystems on the Tibetan Plateau, China. Journal of Integrative Plant Biology 50: 257–264.

Ehleringer JR, Dawson TE. 1992. Water uptake by plants: perspectives from stable isotope composition. Plant, Cell and Environment 15: 1073–1082.

Ehleringer JR, Phillips SL, Schuster WSF, Sandquist DR. 1991. Differential utilization of summer rains by desert plants. Oecologia 88: 430–434.

Ellsworth PZ, Williams DG. 2007. Hydrogen isotope fractionation during water uptake by woody xerophytes. Plant and Soil 291: 93–107.

Fay PA, Carlisle JD, Knapp AK, Blair JM, Collins SL. 2003. Productivity responses to altered rainfall patterns in a C4-dominated grassland. Oecologia 137: 245–251.

Flanagan LB, Ehleringer JR, Marshall JD. 1992. Differential uptake of summer precipitation among co-occurring trees and shrubs in a pinyon-juniper woodland. Plant, Cell and Environment 15: 831–836.

Fowler N. 1986. The role of competition in plant communities in arid and semiarid regions. Annual Review of Ecology and Systematics 17: 89–110.

Li YH. 2010. Response of leaf traits of Nitraria tangutorum Bobr and Nitraria sphaerocarpa Maxim to increasing water. PhD dissertation, Chinese Academy of Forestry. (in Chinese with English abstract)


Liu WJ, Liu WY, Li PJ, Duan WP, Li HM. 2010. Dry season water uptake by two dominant canopy tree species in a tropical seasonal rainforest of Xishuangbanna, SW China. Agricultural and Forest Meteorology 150: 380–388.

Loik ME, Breshears DD, Lauenroth WK, Belnap J. 2004. A multi-scale perspective of water pulses in dryland ecosystems: climatology and ecohydrology of the western USA. Oecologia 141: 269–281.

Ma J, Zheng XJ, Li Y. 2012. The response of CO2 flux to rain pulses at a saline desert. Hydrological Processes 26: 4029–4037.

McCole AA, Stern LA. 2007. Seasonal water use patterns of Juniperus ashei on the Edwards Plateau, Texas, based on stable isotopes in water. Journal of Hydrology 342: 238–248.

Noy-Meir I. 1973. Desert Ecosystems: Environment and Producers. Annual Review of Ecology and Systematics 4: 25–51.

Phillips DL, Gregg JW. 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261–269.

Phillips DL, Newsome SD, Gregg JW. 2005. Combining sources in stable isotope mixing models: alternative methods. Oecologia 144: 520–527.

Schultz NM, Griffis TJ, Lee XH, Baker JM. 2011. Identification and correction of spectral contamination in 2H/1H and 18O/16O measured in leaf, stem, and soil water. Rapid Communications in Mass Spectrometry 25: 3360–3368.

Schwinning S, Ehleringer JR. 2001. Water use trade-offs and optimal adaptations to pulse-driven arid ecosystems. Journal of Ecology 89: 464–480.

Schwinning S, Starr BI, Ehleringer JR. 2005. Summer and winter drought in a cold desert ecosystem (Colorado Plateau) part I: effects on soil water and plant water uptake. Journal of Arid Environment 60: 547–566.

Soriano A, Sala OE. 1983. Ecological strategies in a Patagonian arid steppe. Vegetatio 56: 9–15.

Sun X, Yu Z. 1992. A study on root system of Nitraria tangutorum. Journal of Desert Research 12: 50–54. (In Chinese with English Abstract)

Tian H, Melillo JM, Kicklighter DW, McGuire AD, Helfrich J. 1999. The sensitivity of terrestrial carbon storage to historical climate variability and atmospheric CO2 in the United States. Tellus 51B: 414–452.

White JWC, Cook ER, Lawrence JR, Broecker WS. 1985. The D/H ratios of sap in trees: implications for water sources and tree ring D/H ratios. Geochimica et Cosmochimica Acta 49: 237–246.

Williams DG, Ehleringer JR. 2000. Intra- and interspecific variation for summer precipitation use in Pinyon-Juniper woodlands. Ecological Monographs 70: 517–537.

Xu GQ, Li Y. 2009. Root distribution of three co-occurring desert shrubs and their physiological response to precipitation. Sciences in Cold and Arid Regions 1: 0120–0127.

Xu H, Li Y. 2006. Water-use strategy of three central Asian desert shrubs and their responses to rain pulse events. Plant and Soil 285: 5–17.

Zhou HF, Li Y, Tang Y, Zhou BJ, Xu HW. 2009. The characteristics of snow-cover and snowmelt water storage in Gurbantunggut desert. Arid zone research 26: 312–317. (In Chinese with English Abstract)


Table 1. Morphological characteristics of the three desert shrubs Species Height

(cm) Crown diameter

(cm) Root depth

(cm) Absorbing root area

(cm2) T. ramosissima* 175 ± 13.4 155 ± 17.2 ≈ 300 30249.2 ± 34.3 N. tangutorum 78.3 ± 5.8 328.6 ±18.36 ≤ 200 10622.09 ± 26.4** R. songarica* 55 ± 8.2 35 ± 5.6 ≤ 100 361.8 ± 19.7

Standard error is provided for the mean. * Data are cited from Xu and Li (2009). **Data are cited from Sun and Yu (1992).


Figure 1. Correction curves


Figure 2. IRIS vs IRMS


Figure 3. Precipitation and temperature


Figure 4. Isotopic values of soil water and soil water content


Figure 5. Response of soil water to rainfall pulses


Figure 6. Isotopic values for xylem water


Figure 7. Seasonal changes in water use


Figure 8. Variation in water use after summer rainfall pulse


Figure 9. Variation in water use after spring rainfall pulse


Figure 10


Figure 11. Vertical distribution of the absorbing root area

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Yu Wu , Hai Zhou , Xin-Jun Zheng , Yan Li 1* and Li-Song ... changes in the water use...Knapp, 1995; Tian et al ... Previous studies suggested that the isotopic ... all samples were