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 .