Differential responses of grassland community nonstructural carbohydrate to experimental drought along a natural aridity gradient
Graphical abstract
Introduction
Grasslands cover over 40% of the earth's terrestrial surface and provide many critical ecosystem services, such as soil stability, water conservation, biodiversity, and forage for livestock (Gao et al., 2016). Climate change projections for the 21st century suggest that summer droughts will become more frequent (IPCC, 2013) and grasslands are particularly sensitive to drought (Knapp et al., 2015; Wilcox et al., 2015), given they are primarily water-limited ecosystems (Craine et al., 2012; Hsu et al., 2012; Hoover et al., 2014). Thus, understanding the physiological and community mechanisms by which grasslands respond to drought is important for determining how climate change will impact these essential ecosystems (Smith, 2011).
Many plant physiological responses to drought can be interpreted from measuring non-structural carbohydrates (NSC). Plant NSC are produced during photosynthesis and are essential for maintaining plant metabolism during all life stages (Bouma, 2005; Li et al., 2008a; Hartmann and Trumbore, 2016). Plant NSC are mainly synthesized in leaves from assimilated carbon by photosynthesis and translocated to different organs by mass flow (Du et al., 2020). Given their role in photosynthesis, leaves have higher metabolic activities than roots and stems and therefore store significant portions of the plant's total NSC content (Du et al., 2020; Martinez-Vilalta et al., 2016). Leaf NSCs are used to maintain cell turgor via osmotic adjustment as water becomes limiting (Gersony et al., 2020). When resources are plentiful, NSC production generally exceeds demand, leading plants to store the excess NSC in their vacuoles or plastids for later use (Hartmann and Trumbore, 2016; Ai et al., 2017). During drought, plants reduce stomatal conductance to improve water use efficiency (Chapin et al., 1990), and access stores of NSC to meet metabolic demands (Poorter and Kitajima, 2007; Li et al., 2018c). When stored NSC concentrations fall below a critical threshold required for plant survival, further reductions in water availability can trigger plant mortality and potential shifts in plant community composition (McDowell et al., 2008; Jin et al., 2018). Due to their central role in plant function, NSC dynamics have been used in vegetation models to represent metabolism, species habitat range shifts, plant vulnerability to climate extremes, and even species extinction risks (Rosas et al., 2013). Thus, an in-depth understanding of long-term impacts of drought on community scale NSC is potentially important for forecasting shifts in ecosystem processes and functioning during drought.
To date, much research has focused on assessing NSC responses to drought at the individual species level, whereas such studies are less common at the community scale, especially in grasslands. However, changes in NSC dynamics in response to drought are more relevant to community structure and ecosystem functions when assessed at the community level (Violle et al., 2012). Shifts in plant community NSC concentrations in response to drought can be due to species turnover (i.e., species with different NSC concentrations replacing others and a shift in relative abundance of each species) and/or intraspecific variation (i.e., plasticity and genetic differentiation) in NSC concentrations (Albert et al., 2010; Violle et al., 2012). If shifts in species turnover and intraspecific trait variation in response to drought act in parallel (e.g., species increase NSCs and species with inherently high NSCs become more abundant), then their effects on community NSC dynamics are enhanced (synergistic effects), whereas an opposing shift (e.g., species reduce NSC and high NSC species become more abundant) can be masked in the average community responses (opposing effects). Short-term manipulative drought experiments (i.e., months to years) may impact communities through shifts in both species turnover and intraspecific variation, while observations along natural aridity gradients, which represent long-term exposure to water stress (i.e. decades to centuries), are likely to reveal community functional responses primarily through species turnover (Volf et al., 2016). Therefore, quantifying the relative contributions of species turnover and intraspecific variation is important for understanding the responses of community NSC concentrations to water limitation.
We established a coordinated 4-yr drought experiment at six grasslands sites spanning an aridity gradient in northern China. At each site, we measured plant NSC concentrations of all species cumulatively representing ~90% of total plant biomass to estimate community-weighted mean NSC (NSCCWM) concentrations. The effect of drought on NSCCWM concentrations is influenced by both species turnover (i.e., changes in species relative biomass) and intraspecific trait variability (i.e., changes in species NSC). We tested the hypothesis that experimental drought would have no effect on NSCCWM concentrations due to the opposing effects of intraspecific trait responses (i.e., stomatal closure and reductions in NSC reserves) and species turnover (i.e., increased abundance of drought tolerant species with high NSC concentrations). Additionally, we predicted that NSCCWM concentrations would be maximized at the extremes of the aridity gradient as xeric-adapted species accumulate NSC for osmotic regulation and more productive mesic-adapted species produce more photosynthate (Martinez-Vilalta et al., 2016). This trend would largely be driven by species turnover.
Section snippets
Study sites and experimental design
In 2014, we selected six sites arrayed across the east-west extent of the grassland biome in northern China (see the site names and abbreviations in Table 1). These six sites encompass the three major grassland types in China (i.e. meadow steppe, typical steppe and desert steppe) and vary in mean annual precipitation (MAP), mean annual temperature (MAT), plant species composition and edaphic properties. We extracted climatic variables (e.g., MAT, MAP, and potential evapotranspiration (PET, mm)
Results
Along the aridity gradient, plant SSCWM and total NSCCWM concentrations were lowest at the IMG site with intermediate aridity, and highest at the driest and wettest sites (Fig. 1). In contrast, plant heightCWM and chlorophyllCWM concentration were highest at the intermediate aridity site (Fig. S2). Accordingly, plant SSCWM concentrations were negatively related to plant heightCWM (R2 = 0.79, P = 0.004) and chlorophyllCWM concentration (R2 = 0.68, P = 0.096), and plant total NSCCWM
Discussion
In our study, SSCWM and total NSCCWM concentrations were lowest in the site with intermediate aridity and highest in sites at the opposing extremes of the gradient (Fig. 1). This U-shaped relationship is perhaps due to differences in resource-use tradeoffs exhibited by plants on opposing extremes of the gradient. We document a clear tradeoff between plant investment in acquisitive growth-related traits (e.g., height and chlorophyll) and conservative resource storage traits (e.g., NSC). It is
CRediT authorship contribution statement
W.L. conceived the research; L.S., X.Z., Q.Y., W.M., and J.C. performed experiments; L.S., and W.L. analyzed data and drafted the manuscript, and all authors, especially Z.W., R.J.G., M.H.L., S.L.C., M.D.S., and H.H. contributed to further revising of the text. All authors read and approved the manuscript.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This study was supported by funding from National Natural Science Foundation of China (31971465 and 41603080), Liaoning Provincial Science and Technology Plan Projects (2020JH1/10300006), Strategic Priority Research Program of Chinese Academy of Sciences (XDA23080401), and Youth Innovation Promotion Association CAS (2020199).
References (47)
- et al.
Determination of accurate extinction coefficients andsimultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy
BBA-Bioenergetics
(1989) - et al.
The return of the variance: intraspecific variability in community ecology
Trends Ecol. Evol.
(2012) The spectral determination of chlorophyll-a and chlorophhyll-B, as well as total carotenoids, using various solvents with spectrophotometers of different resolution
J. Plant Physiol.
(1994)- et al.
Responses of non-structural carbohydrates and C:N: P stoichiometry of bothriochloa ischaemum to nitrogen addition on the loess plateauChina
J. Plant Growth Regul.
(2017) - et al.
A multi-trait approach reveals the structure and the relative importance of intra- vs. Interspecific variability in plant traits
Funct. Ecol.
(2010) Understanding plant respiration: separating respiratory components versus a process-based approach
- et al.
Influence of environmental factors on stomatal development
New Phytol.
(2008) - et al.
The ecology and economics of storage in plants
Annu. Rev. Ecol. Evol. Syst.
(1990) - et al.
How plants cope with water stress in the field. Photosynthesis and growth
Ann. Bot.
(2002) - et al.
Responses of two dominant plant species to drought stress and defoliation in the Inner Mongolia steppe of China
Plant Ecol.
(2013)