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.