Varying responses of two Haloxylon species to extreme drought and groundwater depth

Environmental and Experimental Botany 158 (2019) 63–72

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Varying responses of two Haloxylon species to extreme drought and groundwater depth

T

⁎

Xue Wua,b,c, Xin-Jun Zhenga,b,c, , Yan Lia,b, Gui-Qing Xua,b a

State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, Xinjiang, 830011, PR China Fukang Station of Desert Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, Xinjiang, 830011, PR China c University of Chinese Academy of Sciences, Beijing, 100049, PR China b

A R T I C LE I N FO

A B S T R A C T

Keywords: Physiology Stable isotope Water use Groundwater table Extreme drought

In the context of global change, frequent extreme droughts and artificial groundwater overexploitation have significantly changed water availability, which will have profound effects on ecosystem water balance and plant survival. However, few studies have explored the changes in physiology and water-use of desert plants caused by these emerging variations in water availability. Therefore, we investigated the photosynthesis, water potential, and water absorption of two dominant woody species (Haloxylon ammodendron and H. persicum) at three sites with different groundwater depths in the Gurbantunggut Desert of Central Asia during an extreme drought period. Our results showed that: (1) H. ammodendron exhibited more negative pre-dawn leaf water potential and lower photosynthetic capacity (–2.85 MPa, 24.19 μmol CO2 m−2 s−1) than H. persicum (–2.31 MPa, 33.92 μmol CO2 m−2 s−1) during the extreme drought period; (2) pre-dawn leaf water potential and carbon assimilation of H. ammodendron significantly decreased with declining groundwater depths, whereas those of H. persicum were barely affected; (3) both species converted to deeper but different water sources during the extreme drought period: H. ammodendron obtained 56–100% soil water from the near-groundwater layer, while H. persicum obtained 64–100% soil water from the deep soil layer; (4) the depths of water absorption constantly deepened with declining groundwater depths. Variations in water availability have led to the adjustment in plant water uptake, but this adjustment was not sufficient for the optimal physiological performance of H. ammodendron. Thus, under more intense and frequent drought events, further declines in groundwater depth could significantly inhibit growth of this species and may ultimately threaten its survival. Our findings on water use and physiological responses of dominant plant species to decreasing water availability provide a basis for predicting the future of desert plants under deteriorating water conditions.

1. Introduction Dryland, which covers more than 40% of the Earth’s land surface, contributes to approximately 40% of global net primary productivity, and supports over 38% of the total global population (Feng and Fu, 2013; Reynolds et al., 2007), is one of the most sensitive areas to climate change and human activities (Huang et al., 2016; Thomey et al., 2015). Water is fundamental to various biophysical processes that sustain ecosystem functions, including dryland ecosystems, where a tight coupling among ecosystem productivity, surface energy balance, biogeochemical cycles, and water resource availability exists (Hector

et al., 1999; Silvertown et al., 2015). Enhanced warming has intensified the aridity in dryland regions and caused severe and widespread droughts (Dai, 2013; Huang et al., 2012). Changes in land-use and landcover, such as deforestation, irrigation, damming, and groundwater exploitation, have also affected water resource accessibility (Fu, 2003; Gordon et al., 2005). These unprecedented climatic and anthropogenic changes have significantly altered water availability to plants (Piao et al., 2010; Shi et al., 2007), and will have profound effects on ecosystem water balance and plant survival if plants do not acclimate to these novel conditions (Grossiord et al., 2017). Understanding the plant-water relationships under varying water conditions will facilitate

Abbreviations: SWC, gravimetric soil water content; VSWC, volumetric soil water content; Ψpre-awn, pre-dawn leaf water potential; PPFDi, photosynthetic photon flux density; LSP, light saturation point; Pmax, maximum net photosynthetic rate; gs, stomatal conductance; VPD, vapour pressure deficit; δ18Oxylem, δ18O of xylem water; 18 δ Osoil, δ18O of soil water ⁎ Corresponding author at: State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, Xinjiang, 830011, PR China. E-mail address: [email protected] (X.-J. Zheng). https://doi.org/10.1016/j.envexpbot.2018.11.014 Received 2 October 2018; Received in revised form 21 November 2018; Accepted 21 November 2018 Available online 22 November 2018 0098-8472/ © 2018 Elsevier B.V. All rights reserved.

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overexploitation in this area, local water availability has dramatically altered. It remains unclear whether the water use patterns of desert plants will differ under the varying water conditions. Thus, the aim of the present study was to evaluate the water use responses of two dominant woody species (H. ammodendron and H. persicum) to reduced water availability (extreme drought and declining groundwater table depth) and how this would affect their physiological performance. We hypothesized the following: (1) because of water depletion in the upper soil caused by the extreme drought, H. ammodendron and H. persicum must derive water from deeper water reserves, such as deep soil water or groundwater; (2) as H. ammodendron exhibited a higher affinity to groundwater, the physiological activity of this species will be affected by groundwater reduction, while that of H. persicum should be less affected.

in predicting vegetation dynamics and species compositions against the background of future global change. In arid environments, annual precipitation pattern plays a crucial role in determining the composition of plant community (Schwinning and Ehleringer, 2001) and the other major driving force for plant community distribution is the groundwater (Zhang et al., 2018). Both of these are important water sources used by plants for growth and survival. Precipitation in desert ecosystems has three prominent attributes: extremely low quantities, high variability, and unpredictability (Noymeir, 1973). Therefore, soil moisture recharged by precipitation is extremely variable in both space and time (Schwinning and Ehleringer, 2001). In ecosystems with seasonal climates, soil moisture content is high at the beginning of the growing season due to the replenishment from winter and early spring precipitation, while it becomes exhausted in summer because of high temperature and strong evapotranspiration (Donovan and Ehleringer, 1994; Schlesinger et al., 1987). Fluctuations in soil moisture content in space are more rapid and extreme in shallower soil layers, while these fluctuations are relatively slower and moderate at greater depths (Noymeir, 1973). Compared to precipitation, groundwater is a relatively stable and permanent water source, which can be utilized by plants directly, or by supplying root–zone soil water through capillary rise (Fan, 2015; Gries et al., 2003). The utilization of groundwater can help plants to cope with drought (Padilla and Pugnaire, 2007; Zencich et al., 2002). Thus, groundwater has been increasingly perceived as a crucial water source for many plants in terrestrial ecosystems, especially during the dry season (Evaristo et al., 2016; Evaristo and McDonnell, 2017; Fan, 2015). Water use strategies employed by plants are closely associated with rooting depth and root distribution (Brunner et al., 2015; Phillips et al., 2016; Warren et al., 2015). In shallow-rooted plants, the absorbing roots are restricted to the upper soil profile, therefore, they are sensitive to rainfall pulses and exhibit high ability to exploit water stored in the shallow soil layers (Asbjornsen et al., 2008; Cheng et al., 2006). Accordingly, they may experience frequent water stress, because the shallow soil water recharged by precipitation is extremely variable and evaporates easily (Padilla and Pugnaire, 2007). In contrast, the taproots of deep-rooted plants can penetrate several meters below the soil surface, therefore, it is more expensive to maintain. However, the costs associated with carbon and energy consumption can be offset by the advantages that deep roots confer to plants in terms of resource uptake (Pierret et al., 2017). For example, deep roots can obtain nutrient supplies beyond the reach of shallow roots (Silva et al., 2011; ThorupKristensen and Rasmussen, 2015), and allow plants to meet their water requirements by approaching deeper water sources during the drought periods (Ellsworth and Sternberg, 2015; Evaristo and McDonnell, 2017; Zunzunegui et al., 2018). Owing to its utmost importance as a ‘safety net’ against surface stresses, such as drought and soil loss (Maeght et al., 2013; Thorup-Kristensen and Rasmussen, 2015), deep roots have become a common trait among a wide range of plant species in waterlimited environments (Schenk and Jackson, 2002). In addition to the relatively fixed root morphological traits, profuse roots plastic responses also are adaptations to stressful environments (Bonser, 2010; Brunner et al., 2015). In a Haloxylon ammodendron (C. A. Mey.) Bunge population, for instance, more fine roots were distributed in the upper soil profile under favourable water conditions, but they tended to grow deeper when water deficiencies occurred (Xu et al., 2007). Overall, diverse morphological traits and plastic responses of root reflect alternative strategies for plant survival under varying water conditions (Lindh et al., 2014). H. ammodendron and H. persicum Bunge ex Boiss. et Buhse are sister taxa widely distributed in the Gurbantunggut Desert of Central Asia. They are highly valued for ecosystem services such as biodiversity conservation and soil protection against erosion. Based on the isotopic approach, previous studies have revealed the water use strategy of the two species (Dai et al., 2015; Tiemuerbieke et al., 2018). However, due to the changes in precipitation pattern and groundwater

2. Materials and methods 2.1. Study area The study area is located in the south-eastern Gurbantunggut Desert, in the Junggar Basin of Central Asia. Dendritic and honeycomb dunes characterize the landscape, with heights increasing from 5 m at the southern edge to 30 m at the centre. The groundwater table ranges 3–16 m below the ground in the inter-dune low-land. There are two edificators in the community: H. ammodendron and H. persicum. The former grows at the inter-dune low-land, whereas the latter grows at the sand dune. It is a typically temperate continental arid climate with a quite dry and hot summer and a rather cold and snow-covered winter. The annual mean temperature averages 6.6 °C, while annual precipitation and pan evaporation is 70–180 mm and approximately 1000 mm, respectively (Xu et al., 2007). The approximate 25 cm deep snowpack can last 100–150 d stably in winter. A quick snowmelt occurs in early spring, which recharges soil moisture; however, it is then rapidly depleted in the early plant growing season (Zhou et al., 2009). As a result, plants frequently experience soil water deficits in the later growing season. 2.2. Experimental design To investigate the responses of H. ammodendron and H. persicum to groundwater level variations, three sites with different groundwater depths, near the Fukang Station of Desert Ecology, Chinese Academy of Sciences, were selected. The locations coordinates were 44°26′15″–87°54′17″, 44°24′58″–87°54′57″, and 44°21′50″–87°54′54″ (Fig. 1), and the groundwater depths at the locations were 4.0, 6.6, and 11.0 m, respectively. Notably, H. ammodendron and H. persicum had the same groundwater depth at each site, whereas their typical habitats were different. The dune crests, where H. persicum distributed had extremely dry and loose sandy soil, which collapsed inevitably while drilling. Thus, we selected the plants that were closer to inter-dune lowland for easier operation. The distances between these sites were less than 10 km, so that the differences in climatic and physiographic conditions would be negligible. The three study sites were designated as shallow, medium, and deep groundwater sites, respectively. In addition, an extreme drought that occurred in the late summer of 2016 offered the opportunity to understand the responses of the two Haloxylon species to low rain availability. During this severe drought, isotope sampling and physiological monitoring were conducted after a period of 40 consecutive days of no effective precipitation. 2.3. Isotope collection, analysis, and water source calculations Plant xylem and soil samples were collected simultaneously on three consecutive clear days in September 2016. At each site, one set of sunlit and suberized twigs (diameter 0.1–0.3 cm, length 3–4 cm) of each species were sampled from each of four mature and similar-sized 64

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Fig. 1. Location of the three study sites.

period of sampling. Based on the similarities in the δ18O values of soil water (δ18Osoil) in each layer, the soil profile was divided into several sections, and the following three potential water sources were finally identified using a post-integrated method (Phillips et al., 2005):

individuals. Three soil cores were taken next to the sampled plants using a hand auger. Soil samples were collected at 20-cm intervals from the topsoil to groundwater table. All samples were immediately placed into screw-cap glass vials, sealed with Parafilm and stored in a portable cooler to prevent evaporation. A portion of each soil sample was sealed in a tin box to determine gravimetric soil water content (SWC, %) using an oven-drying method. This was converted into volumetric soil water content (VSWC, %) by multiplying the result by the bulk density. Soil and plant xylem water was extracted using a cryogenic vacuum distillation system (LI-2100, LICA, Beijing, China). The extraction tubes were covered by heating devices at 95 °C, and the collection tubes were submerged in liquid nitrogen to freeze/capture the extracted water vapour for isotopic analysis (Barbeta et al., 2015). The total extraction process required apptoximately 2–3 h and the efficiency was over 98%, which was sufficient to obtain unfractionated samples (Yang et al., 2015). The oxygen isotopic compositions of the samples were determined using an isotope ratio infrared spectroscopy analyser – the Liquid Water Isotope Analyser (LWIA, DLT-100, Los Gatos Research Inc., Mountain View, CA, USA), with an analytical precision of individual measurements of ± 0.25‰ for δ18O. The oxygen isotopic composition can be expressed as:

δ 18O = (

Rsample Rstandard

− 1) × 1000‰

(1) Upper soil layer (0–1 m): This component was distinguishable from the rest of the profile as it was the most isotopically unstable zone. (2) Deep soil layer: This component was the intermediate section of the soil profile between the upper soil layer and near-groundwater layer. The isotopic composition of this component was much lower than that of the upper soil layer, and varied mildly. (3) Near-groundwater layer (0–1.5 m above the groundwater table): This component could be identified by a significant increase in SWC and it has a similar isotopic composition to that of groundwater.

2.4. Water potential, photosynthesis, and stomatal conductance measurements All physiological measurements were taken on the same day of isotope sampling at each site. Pre-dawn leaf water potential (Ψpre-dawn, MPa) was measured before sunrise using a model 3005 Pressure Chamber (PMS Instrument Company, Albany, NY, USA). Healthy twigs of randomly selected individuals with no significant mechanical damage were sampled. Five replicates were taken for each species at each site to determine the average value of Ψpre-dawn. The photosynthetic light-response curve was measured in the morning (09:00-14:00) using a Li-6400 portable photosynthesis system (Li-Cor, Lincoln, NE, USA). Photosynthetic photon flux density (PPFDi) was supplied by a 20 × 30 mm2 leaf chamber with a red-blue light source (6400-2B), set as 0, 20, 50, 100, 150, 200, 400, 600, 800, 1200, 1600, 1800, and 2000 μmol m−2s−1. A gas flow rate of 400 μmol s−1 with a 400 μmol mol−1 reference CO2 concentration and a 30 °C of chamber temperature were set to maintain ambient air temperature and relative humidity. At each site, current-year, sunlit twigs from three similar-sized individuals of each species were selected for measurement. The detailed procedures are described in Xu and Li (2006). Net photosynthetic rate and PPFDi were fitted by a modified rectangular hyperbola model to obtain the light saturation point (LSP) and maximum net photosynthetic rate (Pmax):

(1) 18

where Rsample and Rstandard are the oxygen isotopic composition (δ O/ δ16O molar ratio) of the sample and the standard water (Standard Mean Ocean Water), respectively. To eliminate the effect of methanol and ethanol contamination, the δ18O values of the xylem water were corrected by a standard curve created by engineers from Los Gatos (Schultz et al., 2011). Two methods were used to study the water use of the two species. One was the direct inference approach, which directly compares oxygen isotopic composition between the soil water profile and xylem water by plotting them together. The main depth of the soil water sources used by the plants could then be determined based on the depth of soil water with similar δ18O values to the xylem water. The other method was the IsoSource model, which can obtain a feasible range of the different water sources used by plants (Phillips and Gregg, 2003). Source increment was defined as 2% and mass balance tolerance was defined as 0.1‰. With no rains during the 40 days prior to sampling, we did not consider precipitation as an available water source for plants during the 65

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Pn = α

1 − βI I − Rd 1 + γI

presented a decreasing trend, with the average δ18Oxylem at the shallow site was significantly more positive than that at the medium and deep sites, whereas that at the medium site was significantly more positive than that at the deep site (Fig. 4 a). Unlike H. ammodendron, the average δ18Oxylem of H. persicum at the shallow and medium sites were not significantly different but both were significantly more positive than that at the deep site (Fig. 4 b). In the direct comparison, the average δ18Oxylem of H. ammodendron was most similar to the δ18Osoil at depths of 280–340 cm, 520–560 cm, and 960–1000 cm, at the shallow, medium and deep groundwater sites, respectively. The corresponding soil depths for H. persicum were 120–180 cm, 260–360 cm, and 620–840 cm, respectively.

(2)

where Pn is the net photosynthetic rate; I is the PPFDi; Rd is the dark respiration; α is the initial slope of the photosynthetic light-response curve when PPFDi approaches zero, namely the apparent quantum efficiency; and β and γ are coefficients which are independent of I and were obtained by curve fitting (Ye and Yu, 2008). Three replicates were taken for each species at each site to determine the average value of Pmax and LSP. Stomatal conductance (gs) and vapour pressure deficits (VPD) were measured at PPFD = 1800 μmol m−2s−1, using a Li-6400 portable photosynthesis system (Li-Cor, Lincoln, NE, USA). Twelve replicates were taken for each species at each site; in total, 36 measurements were taken for each species. Stomatal sensitivity was calculated using the following equation:

gs = −m lnVPD+ b

3.3. IsoSource estimation of feasible contributions of potential water sources As shown in Fig. 5, neither of the species absorbed much water from the upper soil layers, the contribution of this component averaged only 0.54–3.45% (Fig. 5). At the shallow, medium, and deep groundwater sites, the contributions of the near-groundwater layer for H. ammodendron were in the range of 56–100%, 52–98%, 78–100%, respectively (Fig. 5 a), while the contributions of deep soil water were in the range of 0–44%, 0–48%, and 0–22%, respectively. For H. persicum, the contributions of deep soil layer accounted for 92–100%, 84–100%, 64–100%, respectively (Fig. 5 b).

(3)

where gs is stomatal conductance, b is a reference conductance (b = gsref) at VPD = 1 K Pa and -m quantifies the sensitivity of gs to VPD (Johnson et al., 2012). 2.5. Data analysis Data analyses were performed using SPSS 21.0 (SPSS Inc., Chicago, IL, USA) and charting was processed using the software Origin 8.5 (OriginLab Corp., Northampton, MA, USA). We analysed differences in Ψpre-dawn, Pmax, LSP, and δ18Oxylem using a linear mixed model, in which species and groundwater depth were set as fixed effects. The differences in Ψpre-dawn, Pmax, LSP, and δ18Oxylem in each species among different sites were analysed using one-way analysis of variance (ANOVA) with Fisher’s tests, and the differences in Ψpre-dawn, Pmax, LSP, and δ18Oxylem between H. ammodendron and H. persicum at each site were processed using independent-sample t-tests. Pearson’s correlation was used to test whether stomatal conductance correlated with vapour pressure deficits. P = 0.05 was used to determine statistical significance.

3.4. Leaf water potential There were significant differences in the average Ψpre-dawn between the two Haloxylon species (F = 32.69, P < 0.001) and the three sites (F = 14.56, P < 0.001) (Fig. 6). The average Ψpre-dawn between the two Haloxylon species was not significantly different at the shallow site (N = 5, T = -1.49, P = 0.188), but was significantly different at the medium (N = 5, T = -29.4, P = 0.022) and deep (N = 5, T = -37.98, P < 0.001) sites (Fig. 6). For H. ammodendron, the average Ψpre-dawn at the shallow site was significantly higher than that at the middle and deep sites, and that at the medium site was significantly higher than that at the deep site (Fig. 6). In contrast, the average Ψpre-dawn for H. persicum at the shallow site was significantly higher than that at the middle site but was not significantly different from that at the deep site (Fig. 6).

3. Results 3.1. Volumetric soil water content The VSWC at the three study sites exhibited substantial soil depth variations (Fig. 2). With an increase in soil depth, the average VSWC gradually increased with slight fluctuations, and then increased rapidly when close to the groundwater table (Fig. 2). For H. ammodendron, the average VSWC from the surface to water table was 1.05 to 43.74%, 1.31 to 38.61% and 0.73 to 33.69% at shallow, medium, and deep groundwater sites, respectively. The values for H. persicum ranged from 0.68 to 45.82%, 0.92 to 39.99% and 0.74 to 34.19%, respectively. The average VSWC of the deeper soil layers was remarkably higher than that of the upper soil layers.

3.5. Relationship between stomatal conductance and vapour pressure deficit Correlation analysis showed that there was a significantly negative correlation between gs and ln(VPD) for H. persicum (R2 = 0.207, P = 0.003) (Fig. 7 b), but the relationship for H. ammodendron was not statistically significant (R2 = 0.023, P = 0.648) (Fig. 7 a). The regression equation for H. persicum was y = (0.094 ± 0.029) x + (0.288 ± 0.043) (Fig. 7 b). 3.6. Photosynthesis

3.2. Isotopic compositions of soil water and xylem water

Significant differences in average Pmax and LSP were detected between species (F = 111.53, P < 0.001; F = 39.83, P < 0.001) and sites (F = 6.83, P = 0.009; F = 8.27, P = 0.004) (Fig. 8). At each site, the average Pmax and LSP were significantly different between H. ammodendron and H. persicum (Pmax: N = 3, T = -12.83, P = 0.001; N = 3, T = -11.63, P = 0.007; N = 3, T =-34.34, P = 0.001, at the shallow, medium, and deep sites respectively; and LSP: N = 3, T = -5.52, P = 0.031; N = 3, T = -4.10, P = 0.026; N = 3, T = -5.35, P = 0.033, at the shallow, medium, and deep sites respectively) (Fig. 8). For H. ammodendron, the average Pmax and LSP were significantly different among the three sites (Pmax: F = 59.96, P < 0.001; and LSP: F = 24.89, P = 0.001, respectively), with the largest values at the shallow site and the smallest at the deep site (Fig. 8). However, the average Pmax and LSP for H. persicum were not different among the

Fig. 3 shows the profiles of δ18Osoil and δ18Oxylem at the three studied sites. The δ18Osoil exhibited distinct spatial variations, with the average progressively decreasing with increasing soil depths (Fig. 3). At each site, the δ18Osoil profile was characterized by more positive values in the upper soil layers and more negative values in the deeper soil layers. For H. ammodendron, the average δ18Osoil was more depleted when close to the groundwater table, whereas the average δ18Osoil for H. persicum was more depleted in the deep soil layers (Fig. 3). Fig. 4 shows the δ18Oxylem of the two Haloxylon species. Significant differences in average δ18Oxylem were detected among the three sites (F = 31.24, P < 0.001), but not between the two species (F = 0.14, P = 0.709) (Fig. 4). For H. ammodendron, the average δ18Oxylem 66

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Fig. 2. Vertical profiles of volumetric soil water content of Haloxylon ammodendron and H. persicum at the three sites in the Gurbantunggut Desert where the groundwater depths were 4 m (shallow, a), 6.6 m (medium, b), and 11 m (deep, c). Error bars represent the standard errors of the mean (n = 3).

ammodendron, the result of the present study showed that the neargroundwater layer was the largest contributor, accounting for 52–100% (Fig. 5). Soil water stored in this layer was recharged by the groundwater via capillary rise and thus originated from groundwater. This result suggested that H. ammodendron mainly depended on groundwater during the extreme drought period. This finding is consistent with the results of previous studies conducted at the southern edge of the Gurbantunggut Desert, and only differs in the reported utilization percentage of groundwater. Dai et al. (2014) showed that the contribution of groundwater for H. ammodendron was in the range of

three sites (Pmax: F = 1.29, P = 0.341; and LSP: F = 0.72, P = 0.526, respectively) (Fig. 8). 4. Discussion 4.1. H.ammodendron 4.1.1. Water use Stable isotope analysis provides an effective method to identify the water sources utilized by plants (Ehleringer and Dawson, 1992). For H.

Fig. 3. The δ18O values of xylem water and soil water for Haloxylon ammodendron and H. persicum at the three sites in the Gurbantunggut Desert where the groundwater depths were 4 m (shallow, a), 6.6 m (medium, b), and 11 m (deep, c). Vertical dashed lines represent the mean values of xylem water in H. ammodendron and H. persicum at each site. Error bars represent the standard errors of the mean (n = 3).

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Fig. 4. The δ18O values of xylem water for Haloxylon ammodendron (a) and H. persicum (b) at the three sites in the Gurbantunggut Desert where the groundwater depths were 4 m (shallow), 6.6 m (medium), and 11 m (deep). The different letters indicate significant differences among sites for a given species (P < 0.05), n = 4.

Fig. 6. Pre-dawn leaf water potentials of Haloxylon ammodendron and H. persicum at the three sites in the Gurbantunggut Desert where the groundwater depths were 4 m (shallow), 6.6 m (medium), and 11 m (deep). The different uppercase letters indicate significant differences for H. ammodendron among sites (P < 0.05); the different lowercase letters indicate significant differences for H. persicum among sites (P < 0.05); the asterisks indicate significant interspecific differences at each site (P < 0.05). Error bars represent the standard errors of the mean (n = 5).

Fig. 5. Contributions of potential water sources for Haloxylon ammodendron (a) and H. persicum (b) at the three sites in the Gurbantunggut Desert where the groundwater depths were 4 m (shallow), 6.6 m (medium) and 11 m (deep). Column heights represent the mean value of the relative contributions and bars represent the ranges of minimum/maximum; both were calculated using the IsoSource model. Fig. 7. Correlation between stomatal conductance (gs) and vapour pressure deficit (VPD) of Halooxylon ammodendron (a) and H. persicum (b). The data from three groundwater depths (4, 6.6, and 11 m) were all plotted (n = 36).

68–100% during May-September, Liu et al. (2018) showed that H. ammodendron utilized more than 85% groundwater during May-October, and Lv et al. (2013) showed that the maximum contribution of groundwater for H. ammodendron was 80% in summer. However, Fu et al. (2016) found that H. ammodendron depended on soil water stored at depths of 250–400 cm in July (Fu et al., 2016). This inconsistency could be attributed to age differences in the experimental objects; the experimental plants in the present study were mature adults, while those of Fu (2016) were young individuals without fully-developed root systems. A study conducted on planted H. ammodendron in the Badain Jaran Desert confirmed that H. ammodendron could improve their capacity to use groundwater with increasing age (Zhu and Jia, 2012). Root morphology or architecture is an important determinant of the availability of soil water and thus is closely related to plant-water relationships (Schulze et al., 1996). Previous excavating experiments showed that the H. ammodendron roots could penetrate 10 m below the surface and were distributed in both shallow and deep soil layers (Xu

and Li, 2008; Zou et al., 2010). However, in the present study, the contribution of the upper soil layer (0–100 cm) was extremely low (Fig. 5), which was similar to the observation that H. ammodendron was conservative in using shallow soil water in summer, even following relatively high precipitation (Dai et al., 2015). This limited utilization suggested that the studied species lost the ability to extract water from the upper soil layers. It may result from dehydration or death of fine roots distributed in the upper soil layers due to elevated soil temperatures and depleted SWC during drought periods (Barbeta et al., 2015). Therefore, although rooting depth and distribution define the depth or volume from which plants can potentially extract water (Zencich et al., 2002), water use dynamics are finally determined by root activity, rather than root presence (Wu et al., 2015).

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observations in various forest types, which assumed that plants subjected to drought would explore deeper soil layers to compensate for the low moisture in the topsoil layers (Grossiord et al., 2017). In the studied area, H. persicum grows in sandy soils where water retention is low and there are strong moisture limitations in the topsoil during dry periods. H. persicum, therefore, had to shift water utilization to mitigate the damaging effects of the water stress that occurred in the upper soil layers. The ability to switch rapidly among different water sources could also be advantageous if competition for water occurs within ecosystems (Ehleringer and Dawson, 1992). Unlike H. ammodendron, H. persicum mainly relied on deep soil water, which was recharged by precipitation. The distinct water use patterns may result from the heterogeneity in the topography of their habitats. H. persicum usually grew on the dune crests which are at a greater distance from the groundwater table. Excessive energy costs might prevent its roots from extending to access groundwater (Tiemuerbieke et al., 2018). The soil of dune crests has greater particle size and porosity, permitting snowmelt water or large precipitation to infiltrate rapidly and then be stored in the deep soil layers (Wang et al., 2004). As a result, huge dunes could be regarded as potential water reservoirs that are much easier to access. On the other hand, the horizontal extension distance of the lateral roots of H. persicum was much greater than that of H. ammodendron, allowing it to trap more available water from a larger volume of soil (Zhang et al., 2011). Moreover, previous studies have reported that H. persicum was less tolerant to salinity (Song et al., 2005; Tobe et al., 2000), while groundwater salinity was much higher than that of the soil water (Dai et al., 2015). For these reasons, soil water recharged by precipitation may be a better choice for H. persicum.

Fig. 8. Maximum net photosynthetic rate (Pmax) (a) and light saturation point (LSP) (b) of Haloxylon ammodendron and H. persicum at the three sites in the Gurbantunggut Desert where the groundwater depths were 4 m (shallow), 6.6 m (medium), and 11 m (deep). The different letters indicate significant differences for H. ammodendron among sites (P < 0.05); asterisks indicate significant interspecific differences at each site (P < 0.05). Error bars represent the standard errors of the mean (n = 3).

4.1.2. Physiological responses Seasonal patterns in the Ψpre-dawn of H. ammodendron were found to be closely related to soil moisture (Xu et al., 2011). Assuming equilibrium between plant water potentials and soil water potentials at rooting depth, the decrease of Ψpre-dawn suggested the reduced water availability, implying that H. ammodendron was subjected to more serious water stress at the deeper groundwater site (Fig. 6). According to Yang et al. (2014), the value of Ψpre-dawn corresponding to zero turgor for H. ammodendron was -3.41 MPa, and this was defined as the “survival water threshold” of the growth of H. ammodendron (Yang et al., 2014). In the present study, the lowest Ψpre-dawn measured for H. ammodendron was -3.4 MPa, which was close to the threshold value (-3.41 MPa). This indicates that the normal metabolism of H. ammodendron was likely to be affected by intensified water stress. Meanwhile, decreasing Pmax implied that leaf-scale carbon assimilation was restricted, which meant that the growth of H. ammodendron was heavily inhibited (Fig. 8). The low tissue water potential during drought might constrain cell metabolism and cause stronger stomatal limitation, thereby preventing the production of carbohydrates (Gries et al., 2003; Grzesiak et al., 2013; Craigd et al., 2010). Overall, the pronounced decreasing trends of Ψpre-dawn and Pmax provide sufficient evidence to indicate that groundwater drawdown was associated with decreased physiological activities of H. ammodendron. These results are consistent with those of previous studies conducted in other plant communities, suggesting that the variations in groundwater availability have a great impact on plant physiological performance and even impair the physiological processes (Gries et al., 2003; Horton et al., 2001a, b).

4.2.2. Physiological responses Among the different sites, the average Ψpre-dawn of H. persicum exhibited a little difference, irrespective of groundwater depth variations (Fig. 6). This suggested that groundwater drawdown did not remarkably affect the water status of H. persicum. For H. persicum, a significantly negative correlation was detected between gs and ln(VPD) (R2 = 0.207) (Fig. 7), suggesting that H. persicum was highly sensitive to atmospheric desiccation. Thus, the relatively stable water status of H. persicum might be attributed to high stomatal sensitivity, as its stomata responded to increasing VPD through partial closure, representing a conservative water use strategy. Another noteworthy observation was that there was no significant difference in the average Pmax and LSP among the three study sites (Fig. 8), suggesting that H.persicum could maintain stable carbon fixation under varying water conditions. In this regard, the generally superior water status could partly be responsible for the photosynthetic consistency. Moreover, effective osmotic adjustments may also play a crucial role in explaining this, since osmosis of organic molecules, such as ABA, proline, and soluble sugar, were the most important factors in plants that undergo adjustments to resist water stress (Song et al., 2006). When soil and plant water conditions altered, osmotic adjustment operated to maintain a stable turgor pressure of the leaf cells, and thus contributed to maintaining stomata opening and normal photosynthesis at the leaf scale (Xu and Li, 2006). The high-photosynthesis and high-water potential characteristics of H. persicum evidenced in the present study are consistent with the results of a previous study that H. persicum was a typical drought-resistant species existing in desert environments (Jiang, 1992). In summary, the relatively stable leaf water potential and high photosynthetic rates demonstrated that groundwater drawdown had less influence on the physiology and growth of H.persicum. Deep soil water appeared to be sufficient for optimal performance and water balance of H. persicum under the varying water condtions. High stomatal sensitivity and effective osmotic regulation of H. persicum might also play essential roles.

4.2. H. persicum 4.2.1. Water use The seasonal water uptake pattern of H. persicum has already been clearly determined; this species extracts shallow soil water recharged by snowmelt water during early spring and reverts to deeper water sources during dry summer periods (Dai et al., 2015; Tiemuerbieke et al., 2018). In the present study, isotopic analysis showed that the largest contributor for H. persicum was the deep soil layer component, in the range of 64–100% (Fig. 5). It was consistent with the previous results, suggesting that H. persicum mainly relied on deep soil water during the extreme drought period. This agreed with numerous 69

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depending on soil water converted by unpredictable precipitation, H. persicum was more sensitive to atmospheric drought, as indicated by the significant correlation between gs and ln(VPD) (R2 = 0.207) (Fig. 7), it therefore could maintain a stable water status and carbon accumulation regardless of the groundwater limitation. The results in the present study indicate that diverse traits were functionally related and defined two different eco-physiological responses and water use strategies in H. ammodendron and H. persicum. These species-specific responses are likely to aid in buffering against the negative effects of climate change (Barbeta et al., 2015).

4.3. Comparison During the dry period, both H. ammodendron and H. persicum exploited deeper water sources, such as groundwater or deep soil water, which confirmed our first hypothesis. This suggested that both the studied species possessed deep root systems that enabled them to reach available water sources. Deep roots could be considered as insurances against the potential consequences of drought under less favourable conditions (Pierret et al., 2017). In water-limited environments, many plants employ deep rooting strategies to avoid the water deficiency which occurs in the upper soil layers and thereby survive longer during rainless periods (Nardini et al., 2016; Wu et al., 2015; Zencich et al., 2002). Although the two species in the present study possess similar root patterns, they exhibited a significant difference in the extraction of water sources, with H. ammodendron deriving the majority of water from the near-groundwater layer, while H. persicum dominantly using water stored in the deep soil layer above the groundwater table. Essentially, H. ammodendron had a stable water source, groundwater, whereas H. persicum relied more on an unstable water source, precipitation. This was consistent with the results of previous studies, which showing that the two species had different water use patterns (Dai et al., 2015; Tiemuerbieke et al., 2018). When the lowest leaf water potentials were measured, the δ18Oxyelm of H. ammodendron were the most depleted (Figs. 6 and 4). The association of the lowest Ψpre-dawn with the most depleted δ18Oxyelm implied the water use strategy of H. ammodendron, extracting water resources from deeper soil layers when drought conditions were exacerbated during dry days. This was consistent with the results estimated through the IsoSource model that H. ammodendron switched water absorption to deeper soil depths with the declining groundwater depths. Although H. persicum is not a groundwater-dependent plant, the overall trend of water absorption depths observed along the groundwater depth gradients was consistent with H. ammodendron, which was constantly moving deeper. This trend corresponded to the results of a root distribution investigation conducted in the Gurbantunggut Desert, where H. persicum plants at the deepest groundwater depth developed larger root surface areas and rooted more deeply compared to the individuals at the shallowest groundwater site (Xu et al., 2017). Variations in water uptake depths suggested that more production of absorbing roots were stimulated in deeper soil layers where water was abundant (Barbeta et al., 2015). This supported the common assumption that plants could increase carbon allocation to promote roots to grow deeper in the soil under conditions of soil water depletion (Grossiord et al., 2017; Schwinning and Ehleringer, 2001). This change in water utilization can be considered as an adjustment of plants to adapt to novel conditions through root phenotypic plasticity, which is important to species evolution (Nicotra et al., 2010). H. ammodendron and H. persicum are sister taxa growing on adjacent habitats in the Gurbantunggut Desert, but they displayed significant interspecific physiological differences. For example, H. persicum kept a more superior water status than H. ammodendron, in terms of the more positive Ψpre-dawn (Fig. 6), although SWC was higher for H. ammodendron (Fig. 2). Additionally, H. persicum had much stronger photosynthetic capacity and could better utilise strong light, as indicated by much higher average Pmax and LSP (Fig. 8). According to Mazer et al. (2010), consistent differences in the physiological performance of wild populations of closely related plant taxa might be the result of environment induced phenotypic plasticity or adaptive evolution, or a combination of the two. In addition to the inherent differences, root water uptake also plays an important role in plants’ physiological performances (Zunzunegui et al., 2018). As groundwater-dependent plants, stomatal regulation of H. ammodendron was unresponsive to atmospheric desiccation but more responsive to hydrological drought, as indicated by decreasing Ψpre-dawn. Consequently, when declining groundwater depths resulted in accelerated water deficiency, carbon assimilation of H. ammodendron was severely inhibited. However,

4.4. Implications In the studied area, groundwater is mainly converted from surface water, including 14% direct replenishment, such as precipitation infiltration, and 86% indirect replenishment, such as channel leakage and field infiltration (Deng, 2009). With regard to global climate change, increasing temperature and precipitation have been recorded in the last 50 years for this region (Li et al., 2013), but precipitation is easily lost from the soil because of strong evaporation effects. This typical arid climate characteristic determines that precipitation infiltration contributes little to groundwater recharge. Meanwhile, with the prevalence of water saving techniques, many seepage prevention channels were widely constructed, resulting in reduced recharge to groundwater from oasis farmlands. Drip-irrigation techniques greatly stimulated large areas of land reclamation, and local farmers pump groundwater to meet the irrigation requirement. These anthropogenic practices caused major effects on the groundwater system and led to dramatic groundwater drawdown in the studied area, at the rate of 0.38–0.92 m/year (Du et al., 2013). Therefore, the valuable groundwater resource has become a major restricting factor of local economic development, living standards, and the ecological security of oasis farmlands (Chen, 2017). H. ammodendron is the most important species in the Gurbantunggut Desert, not only because it represents the dominant species, but also because of its indispensable ecological functions. Its roots are the principal stabilizing element in this arid region, providing the final barrier against the encroaching deserts in the marginal oasis. H. ammodendron has been reported to suffer from ongoing habitat shrinkage and extensive degradation due to groundwater drawdown, especially when the depth was greater than 8 m (Zeng et al., 2012). The present study further revealed the mechanism underlying these negative effects, namely, that groundwater drawdown is associated with the watercarbon imbalance of H. ammodendron. Although H. ammodendron has actively adjusted its root distribution to explore more available water in deeper soil layers, this water utilization shift unfortunately could not offset the adverse effects on its physiological activities, thereby limiting carbon gain severely. Carbon assimilation and allocation are the fundamental processes determining plant growth, development, survival, reproduction, and defence (Carnicer et al., 2013). Once this pivotal process is disturbed, it may lead to serious consequences associated with population dynamics and compositional changes (Martin-StPaul et al., 2013). Therefore, groundwater drawdown is detrimental to the growth of H. ammodendron, and even endangers its future subsistence through longer-term processes. In view of its important ecological significance, it is urgently required to frame and implement effective measures based on the sustainability of groundwater resources to protect H. ammodendron. Author contribution Xin-Jun Zheng conceived the idea and supervised the research work. Gui-Qing Xu provided conceptual advice. Xue Wu conducted the experiments, analysed the data and drafted the manuscript. Yan Li provided critical review and edited the manuscript. All authors read and approved the final manuscript. 70

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Conflict of interest

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