Introduction
Arid regions occupy approximately 30% of the Earth’s land surface and are occupied by almost 1 billion people (Yin et al., 2013; Yin et al., 2015). The ecosystems in these regions are substantially more fragile than most owing to dry infertile soil, resulting in poor vegetation cover (J. Huang, Yu, Guan, Wang, & Guo, 2016; Reynolds et al., 2007). Native vegetation plays an important role in keeping these environments suitable for socioeconomic development and human habitation by providing natural protection against desertification and reducing poverty and food insecurity (Reynolds et al., 2007; Schreckenberg et al., 2006). Because of low rainfall accompanied by high evapotranspiration in these inland regions, groundwater is often an important water source for natural vegetation, agricultural practices, domestic use, and public drinking (Fan, Li, & Miguez-Macho, 2013; F. Huang, Zhang, & Chen, 2019). In recent years, the vegetation of inland groundwater-dependent terrestrial ecosystems (GDEs) has been increasingly recognized for its ecological and socio-economic values (Froend & Sommer, 2010; Thomas et al., 2006). However, anthropogenic withdrawal of groundwater for expanding agricultural and domestic use, coupled with climate change-related drought (Ashraf et al., 2017; Taylor et al., 2013), had lead to the depletion of groundwater reserves and resulted in groundwater decline, hence severely limiting water availability for inland vegetation (Glazer & Likens, 2012; Orellana, Verma, Loheide, & Daly, 2012). GDEs are at risk of degrading, which has become of increasing concern, due to uncertainties about how vegetation will respond to changing groundwater conditions on short and long term timescales (Antunes, Chozas, et al., 2018; Antunes, Díaz Barradas, et al., 2018).
Plant functional traits are important in determining differential tree mortality in response to drought (O’Brien et al., 2017), and trait-based methods have proven effective in identifying changes to water availability due to precipitation gradients or altitudinal variations (Rosado, Joly, Burgess, Oliveira, & Aidar, 2016). However, these methods have been applied to tropical rainforest plants where rainfall is plentiful; whereas, woody, perennial phreatophytes that are supported by shallow groundwater aquifers (Wu, Zheng, Li, & Xu, 2019; Yin et al., 2015; Zhou, Zhao, & Zhang, 2017) make up the majority of natural vegetation in arid regions (Sommer & Froend, 2011; Thomas, 2014). The resilience of these ecosystems to changing hydrological and climatic conditions depends largely on the capacity of phreatophytic plants to cope with reduced groundwater availability (Hultine et al., 2020). Understanding the physiology of woody phreatophytes to decreases in groundwater level is considered to be a major unresolved question in GDEs (Eamus, Zolfaghar, Villalobos-Vega, Cleverly, & Huete, 2015; Orellana et al., 2012). Previous studies have focused on groundwater fluctuation (flood inundations, experimental alterations, or distances to main river channels) on desert riparian forest performance (Li et al., 2019; Pan, Chen, Chen, Wang, & Ren, 2016). However, the effects of variation in groundwater on non-riparian phreatophytes remains unclear (Wu, Zheng, Yin, et al., 2019), despite the affected areas being very large (Cooper et al., 2006).
Access to groundwater plays an important role in determining plant function and survival in GDEs (Froend & Sommer, 2010; Zolfaghar, Villalobos-Vega, Cleverly, & Eamus, 2015). Depth to groundwater (DGW) further influences leaf water relations, hydraulic properties, growth, productivity, survival, and species composition (Gries et al., 2003; Griffith, Rutherford, Clarke, & Warwick, 2015; Yang, Li, Li, & He, 2019; Zolfaghar et al., 2014). Plasticity in hydraulic architecture plays a central role in adapting to differences in water availability (Tyree & Ewers, 1991; Zolfaghar, Villalobos-Vega, Zeppel, & Eamus, 2015). By affecting the rate of water flow through xylem, hydraulic architecture potentially influences water potential (Ψ ), stomatal conductance, rate of photosynthesis and growth (Awad, Barigah, Badel, Cochard, & Herbette, 2010; Carter & White, 2009; Zeppel & Eamus, 2008). Huber value, xylem vulnerability to embolism, and hydraulic safety margins are key components of hydraulic architecture (Carter & White, 2009; Hubbard, Ryan, Stiller, & Sperry, 2001). Understanding how these traits change across gradients of water availability (DGWs) is important for predicting the fates of xeric phreatophytes facing groundwater decline (Antunes, Díaz Barradas, et al., 2018). Currently, few studies have assessed the response of intraspecific hydraulic architecture to variations in DGW (Garrido et al., 2020; Lucani, Brodribb, Jordan, & Mitchell, 2019).
Osmotic adjustment protects against declining water availability by counteracting turgor loss (Burgess, 2006; Cushman, 2001; Si, Feng, Yu, Zhao, & Li, 2015). Pressure–volume (P-V) analyses have revealed that osmoregulation increases drought resistance as DGW increases (Zolfaghar, Villalobos-Vega, Cleverly, et al., 2015). By increasing and maintaining higher levels of intracellular compatible solutes, osmotic adjustment enhances the capacity for turgor maintenance (Cater, 2011; Gebre, Tschaplinski, Tuskan, & Todd, 1998; Nolan et al., 2017) via active accumulation of in/organic solutes in cells in response to deceases in the cellular environment’s Ψ . Declining cell osmotic potential (π) further attracts water into cells maintaining turgor pressure (Cater, 2011; Si et al., 2015). However, attributes that confer the capacity to tolerate water stress (lower saturated turgor) may limit growth potential under favorable water conditions (Chen et al., 2015; Fernandez & Reynolds, 2000; Leuschner, Wedde, & Luebbe, 2019). Increasing DGW limits the growth of woody phreatophytes (Gries et al., 2003; J. Li et al., 2013), but how do groundwater-dependent woody phreatophytes survive hydrological drought conditions and what drives that osmoregulation (Kroeger, Zerzour, & Geitmann, 2011)? To our knowledge, the effects of increasing DGW on plant growth through cell turgor regulation has never been tested.
Haloxylon ammodendron (C.A. Mey.), a small non-riparian, xeric phreatophytic tree, is endemic to desert regions of Asia and Africa (Thomas, 2014; G.-Q. Xu, McDowell, & Li, 2016). Our early research showed several morphological adjustments (decreases in assimilation-related branch areas and assimilation-related branch growth rates) that are important drought acclimation strategies to ensure normal photosynthesis and survival of H. ammodendron during summer droughts (H. Xu, Li, Xu, & Zou, 2007). As a succulent and xero-halophytic shrub, osmotic adjustments are also important forH. ammodendron ’s success in a drought environment, as mediated through Na+, soluble sugar, and proline (Lu et al., 2019; Zheng, Xu, Li, & Wu, 2019). Moreover, during the extreme summer drought period, H. ammodendron uses deeper water sources, while the depth of the water absorption deepens as groundwater depth declines (Wu, Zheng, Li, et al., 2019). Therefore, absorbing water from deeper soils may influence water budgets, hydraulic properties, and growth rates at the leaf and branch levels (Canham, Froend, & Stock, 2009; Zolfaghar et al., 2014). Yet, the influence of DGW on hydraulic properties and the trade-off between drought tolerance and growth are not clear. Here, we compared xeric phreatophytes under the same meteorological conditions that provided an opportunity to compare intra-specific variation in hydraulic architecture across sites having differential access to groundwater. The aims of this study were to: 1) elucidate differences in hydraulic performance across sites with different DGW, 2) asses drought resistance at greater DGW, and 3) reveal the major active osmoregulation compounds responsible for influencing growth in H. ammodendron .