Abstract
Quantifying interspecific variations of tree resilience to drought and
revealing the underlying mechanisms are of great importance to the
understanding of forest functionality particularly in water-limited
regions with foreseeable increase in temperature and the associated
drought stress. So far, comprehensive studies incorporating
investigations in interspecific variations of long-term growth patterns
of trees and the underlying physiological mechanisms are very limited.
Here, in a semi-arid site of northern China, tree radial growth rate,
inter-annual tree-ring growth responses to climate variability, as well
as physiological characteristics pertinent to xylem hydraulics, carbon
assimilation and drought tolerance were analyzed in seven pine species
growing in a common environment. Considerable interspecific variations
in radial growth rate, growth response to drought and physiological
characteristics were observed among the studied species. Higher
hydraulic efficiency is related to greater photosynthetic capacity but
not higher tree radial growth rate. Rather, radial growth of species
with higher hydraulic conductivity and photosynthetic capacity was more
sensitive to drought stress that is at least partially due to a
trade-off between hydraulic efficiency and safety across species. This
study thus demonstrates the importance of drought resilience rather than
instantaneous
water and carbon flux capacity in determining tree growth in
water-limited environments.
Keywords: cavitation, drought, embolism, growth resilience,
hydraulic, photosynthesis, pine, radial growth, tree-ring, xylem
Introduction
Climate-change related drought events have been observed with increasing
frequency and intensity in recent decades, causing serious adverse
effects on many forest ecosystems worldwide (Allen et al., 2010; Dai,
2011; McDowell et al., 2008). Widespread reductions of tree growth and
increased forest decline or even mortality triggered by drought have
been reported, particularly in water-limited environments (Gitlin et
al., 2006; Rigling et al., 2013;
Sun
et al., 2019). Physiological differences among tree species can
potentially lead to large interspecific variation with respect to
responding to the warming-drying trend of climate change (Adams et al.,
2017; Anderegg et al., 2015; Gazol et al., 2018; Zang, Hartl-Meier,
Dittmar, Rothe, & Menzel, 2014). A large number of data on tree
responses to droughts have been accumulated by tree-ring analyses in the
past few decades, which have laid an important foundation for
understanding the impacts of climatic change on forest ecosystems
(Gazol, Camarero, Anderegg, & Vicente-Serrano, 2017; Lloret, Keeling,
& Sala, 2011; Wu et al., 2017). However, physiological mechanisms
underlying the observed patterns from tree-ring analyses are much less
investigated, which limited our ability in assessing the risk of forest
decline and mortality under the influence of climate change (Allen et
al., 2010; Li et al., 2020b).
Tree radial growth is sensitive to annual climatic variation, especially
in the water-limited environments like arid and semi-arid regions
(DeSoto et al., 2020; Fritts, 1976; López et al., 2013). In general,
tree radial growth decreases during droughts and recovers upon
subsequent significant rainfall events, although large differences in
climatic sensitivity exist among species (DeSoto et al., 2020; Fang &
Zhang, 2018; Wu et al., 2017). Growth performance of different tree
species in water-limited environments may strongly depend on their
resistance to drought and recovering ability from climatic disturbances,
which reflect species’ ability in maintaining their physiological
functions during and after droughts (Anderegg et al., 2013;
Manrique-Alba et al., 2018). Tree sensitivity to drought stress has been
found to be strongly associated with growth rate in many forest
ecosystems, that is, fast-growing tree species usually have low
resistance to drought stress but can recover more quickly from drought
disturbances, and vice versa (Choat et al., 2012; Gazol et al., 2018;
Zhang et al., 2014). A trade-off between drought resilience and growth
rate across species has often been observed in water-limited
environments
(Gazol
et al., 2017;
Martínez-Vilalta,
López, Loepfe, & Lloret, 2012). Characterizing growth responses of
different tree species to non-lethal drought events is crucial for
predicting tree growth performances and mortality risks in facing
increasing climatic
variability
(DeSoto et al., 2020; Lloret et al., 2011; Zhang et al., 2014).
Tree-ring analysis provides a retrospective picture to characterize
inter-annual variation of tree growth and its relationship with climate
variables (Gazol et al., 2017; Lloret et al., 2011). The sensitivity of
tree-ring growth to climate variability among species is usually
presented by variations of their inter-annual ring width, which is
strongly related to tree radial growth rate and resilience to drought
events (Macalady & Bugmann, 2014; Taeger, Zhang, Schneck, & Menzel,
2013). Tree-ring analyses can also play an important role in
characterizing tree growth rates and risks of tree mortality during and
after extreme drought events (DeSoto et al., 2020; Gazol et al., 2017;
Lloret et al., 2011). Recently, tree-ring analyses have been used to
intuitively show interspecific difference in growth responses to drought
events using three indices, i.e. tree resistance (RT), tree recovery
(RC) and tree resilience (RS). Previous studies have shown that growth
resilience varies greatly among species that is assumed to be influenced
by the specie-specific physiological
response
to drought events (Anderegg et al., 2015; Gazol et al., 2017,
2018).
However, studies directly linking tree-ring analyses with physiological
functional traits are scarce, which hinders our ability in foreseeing
tree growth decline and mortality in facing increasing drought.
Physiological
functions influence tree radial growth in many aspects, including
through photosynthesis rate and respiration rate, or indirectly through
plant water relations (Chaves, Flexas, & Pinheiro, 2008; Hubbard, Ryan,
Stiller, & Sperry,
2001).
Drought-induced xylem cavitation will reduce hydraulic conductance, and
thus, negatively impact on photosynthetic gas exchange and ultimately on
tree radial growth (Brodribb, Holbrook, & Gutiérrez, 2002; McDowell,
2011; Rehschuh et al., 2020). Pines are known to reduce their stomatal
conductance under drought stress, maintaining relatively constant
minimum leaf water potentials to avoid the risk of hydraulic failure,
although this unavoidably comes at a cost of reduced carbon assimilation
and hence reduction in growth (McDowell et al., 2008; Meinzer et al.,
2016; Tyree & Sperry, 1988). This isohydric water management strategy
can contribute to avoidance or delay of catastrophic hydraulic failure
due to xylem embolism; however, carbon starvation can happen and cause
mortality if drought stress sustains (McDowell et al., 2008; Sala,
Piper, & Hoch, 2010). Nevertheless, even among closely related pine
species, interspecific variations in hydraulic architectural
characteristics can exist and thus lead to different growth responses to
drought (e.g. Herguido et al., 2016; Li et al.,
2020a).
According to the theory of plant ‘fast–slow’ economics spectrum,
species with high water transport capability usually have low tissue
density, short tissue life span and high rate of resource acquisition
(Reich, 2014). Physiological functional traits associated with high rate
of resource acquisition and processing are usually inversely correlated
with drought resistance traits across species. Consistently, a trade-off
between xylem water transport efficiency and safety against
drought-induced embolism has long been hypothesized and widely observed
(Brodribb, Bowman, Nichols, Delzon, & Burlett, 2010; De Guzman,
Santiage, Schnitzer, & Álvarez-Cansino, 2017; Martínez-Vilalta, Prat,
Oliveras, & Piñol, 2002). Although this hydraulic efficiency-safety
trade-off can be weak at the global scale (Gleason et al., 2016), it has
been commonly observed in specific sites (Martínez-Vilalta et al., 2002;
Pockman & Sperry, 2000) and among particular taxa (De Guzman et al.,
2017; Fan, Zhang, Hao, Ferry, & Cao, 2012). This trade-off can largely
be attributed to biophysical constraints to xylem formation that do not
allow high efficiency and high embolism resistance at the same time (Fan
et al., 2012; Hao et al., 2013; Pockman & Sperry, 2000; Wheeler,
Sperry, Hacke, & Hoang, 2005).
Hydraulic
functional traits of trees are fundamentally linked to their
environmental fitness and thus may help to predict tree performances in
terms of radial growth and response to drought (Reich, 2014). The
combination of tree-ring analyses and measurements of hydraulic
functional traits has great potential in identifying the patterns of
species-specific growth performances and meanwhile revealing the
underlying physiological mechanisms of such interspecific variations.
Tree growth conditions are expected to exacerbate in large areas all
over the world, including vast areas of northern China, as increasingly
stronger drought could be foreseen in the coming decades (Choat et al.,
2018; Dai, 2011; Williams et al., 2013).
In
natural ecosystems, climate change is expected to induce significant
shifts of population composition and forest structure since the climatic
conditions may become unsuitable for some species while being more
suitable for some others (Adams et al., 2017; DeSoto et al., 2020).
Similarly, tree species that are commonly used for afforestation
nowadays may become unsuitable in the near future due to the fast
climate change (Montwé, Spiecker, & Hamann, 2014; Way & Long, 2015;
Verkerk et al., 2020). Actually, widespread and severe decline and
mortality of some drought sensitive tree species widely used for
creating large-scale plantations have been observed in recent years
(Kang, Zhu, Li, & Xu, 2004; Liu et al., 2018; Sun et al., 2019; Tausz,
Merchant, Kruse, & Samsa, 2008). Investigations on the interspecific
differences in tree growth responses to drought as well as the
underlying mechanisms are of great importance in forestry under the
background of fast climate change (Anderegg et al., 2015; Wu et al.,
2017). At the semi-arid regions of northern China, water stress is a
dominant limiting factor for tree growth and survival of pine species,
which are often used for creating plantations particularly in areas with
sandy soil (Liu et al., 2018; Zhu, Fan, Zeng, Jiang, & Takeshi, 2003).
Here, using seven pine species growing in a common environment in a
typical semi-arid area with sandy soil, we tried to identify the
interspecific differences in growth patterns in relation to limiting
climate factors as well as to reveal the underlying physiology causing
such variations particularly from the point of view of xylem hydraulics
and leaf water relations. Specifically, we hypothesized that: 1) the
pine species with high hydraulic conductance would have high radial
growth rate considering the commonly observed positive correlation
between xylem water transport efficiency and photosynthetic carbon
assimilation; 2) species with characteristics related to greater
resistance to drought-induced xylem embolism and leaf traits reflecting
greater drought tolerance would show greater resilience to droughts
during climatic extremes; 3) a trade-off between hydraulic efficiency
and safety would result in greater sensitivity in tree radial growth to
extreme droughts in species with intrinsically high hydraulic capacity.