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doi:10.1093/treephys/tpu088

Integrating plant hydraulics and gas exchange along the drought-response trait spectrum

Stefano Manzoni1

Department of Physical Geography and Quaternary Geology, Stockholm University, Svante Arrhenius väg 8C, Frescati, SE-106 91 Stockholm, Sweden; 1Corresponding author (stefano.manzoni@natgeo.su.se)

Received September 9, 2014; accepted September 24, 2014; handling Editor Danielle Way

Vegetation responses to environmental conditions are mediated by a suite of functional traits affecting water relations, resource acquisition and other aspects of plant function. Functional traits exhibit strong coordination within and across species, thereby defining strategies that are broadly aligned along trait spectra (Reich 2014). The hypothesis proposed to explain these pat-terns is that coordination allows the most efficient resource exploitation and allocation, thus improving fitness (Maire et al. 2013, Manzoni et al. 2014b, Prentice et al. 2014). The leaf econ-omy spectrum links strategies associated with contrasting leaf morphologies, nutrient contents, leaf lifespans and photosyn-thetic capacities (Wright et al. 2004). Climatic conditions have been shown to only weakly affect where species are located along this spectrum, indicating that a range of strategies can coexist under a given climate (Wright et al. 2005). Because leaf functioning critically depends on the supply of water and nutri-ents, leaf and stem traits (in particular hydraulic traits) are also expected to be coordinated (Reich 2014). Indeed, the maximum hydraulic conductances of stems and leaves are correlated with the maximum stomatal conductance (Mencuccini 2003, Sack et al. 2003, Manzoni et al. 2013b), and these conductances scale with gas exchange rates and photosynthetic capacity (Brodribb and Feild 2000, Katul et al. 2003, Brodribb et al. 2007, Prentice et al. 2014). These broad patterns link the plant carbon, nutri-ent and water economies under ‘average’ conditions, but do not track trait responses to environmental stresses. Developing a deeper understanding of drought-response strategies and their organization along a spectrum of drought-response traits raises the question of whether the rates of decline of functional traits during drought are coordinated in the same manner as the ‘aver-age’ trait values. This question is addressed in this issue of Tree

Physiology by Zhou et al. (2014b), who quantified the rates of decline of stomatal conductance, carboxylation capacity, maxi-mum electron transport rate and mesophyll conductance in nine tree species along a marked hydro-climatic gradient.

As the soil dries, transpiration decreases due to reductions in the hydraulic conductances of all compartments along the soil–plant–atmosphere system, i.e. (i) in the soil volume sur-rounding the roots; (ii) within the plant xylem (cavitation and air embolism); and (iii) at the leaf–atmosphere boundary (sto-matal closure) (Cruiziat et al. 2002, Manzoni et al. 2013b). Several plant traits are involved in the regulation of water transport through these compartments, including the hydrau-lic conductances of xylem and extra-xylary pathways to liquid water, and stomatal conductance. The argument that hydraulic traits should be coordinated to improve fitness under ‘average’ growth conditions could be extended to drought conditions, leading to the hypothesis that the rates of decline of different functional traits during drought are also coordinated. The water potential at 50% loss of xylem conductivity (ψ50,X) indeed co-varies with the minimum stem and leaf water potential, sug-gesting that stomatal closure is coordinated with the loss of conductivity (Meinzer et al. 2009, Choat et al. 2012), as con-firmed by comparisons between xylem vulnerability and stoma-tal closure curves (Cruiziat et al. 2002, Brodribb et al. 2003). Different degrees of coupling between conductances result in varying relations between soil and leaf water potentials, so that near-isohydric behavior ensues when xylem and stoma-tal conductance decreases in concert, whereas slower stoma-tal closure compared with xylem conductivity losses leads to anisohydric behavior (Martínez-Vilalta et al. 2014). Therefore, coordination of xylem conductivity loss and stomatal closure is

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a pre-condition for the canopy water potential to remain within non-stressful bounds and avoid desiccation.

Carbon uptake also decreases during dry periods, partly due to stomatal closure and partly because of decreased diffusivity in the mesophyll and metabolic limitations to pho-tosynthesis (Flexas et al. 2004, Lawlor and Tezara 2009). Mesophyll and stomatal conductances decrease simultane-ously during drought and the impairment of photosynthetic capacity increases as water stress progresses (Flexas et al. 2004, Galmes et al. 2007, Warren 2008; but see a critique of mesophyll conductance estimation approaches by Gu and Sun 2014). However, evidence for simultaneous changes in meso-phyll conductance, stomatal conductance and photosynthetic capacity across species and ecosystems has been limited. In this issue, Zhou et al. (2014b) showed positive correlations among the rates of decline of these parameters as the experi-mental drought progressed, thereby defining a spectrum of drought responses from more resistant species thriving in dry

environments to more sensitive species from moist environ-ments, which exhibit reduced gas exchange and strong meta-bolic limitations early during soil drying.

Because correlations have been established between the rates of decrease of xylem and stomatal conductances, and between the rates of decrease of metabolic capacity and sto-matal conductance, it might be argued that all three sets of traits are coordinated. To illustrate this multivariate coordina-tion, published trait data were collected and are summarized in Figure 1. Water potential values at 50% stomatal closure (ψ50,S) and 50% reduction in metabolic activity (ψ50,M) in Figure 1a were obtained by elaborating literature data from Manzoni et al. (2011) and employing data from Zhou et al. (2014b). The former dataset was used to estimate the ‘apparent’ maxi-mum carboxylation capacity (Vc,max′ in Zhou et al.'s notation) by inverting the light-saturated photosynthesis– internal CO2 concentration (A–ci) curve at the working point, for different degrees of soil drying (following the approach by Katul et al.

2 Manzoni

Figure 1. Coordination of drought-response strategies in woody species worldwide, expressed as co-variation of three functional traits—the water potential levels at 50% stomatal closure (ψ50,S), 50% loss of xylem conductivity due to cavitation (ψ50,X) and at 50% reduction of metabolic activ-ity (ψ50,M, where metabolic activity is expressed as apparent maximum carboxylation capacity, Vc,max′). The three panels illustrate bivariate scatter plots of all the combinations of these three traits. Color and symbols identify different biomes; open large, open small and filled large symbols, respectively, refer to deciduous angiosperms, evergreen angiosperms and gymnosperms. Thick dashed lines are reduced major axis regressions of the log-transformed data; thin dot-dashed lines are 1 : 1 lines; in each plot the number of data points (n), the correlation coefficient (R), the prob-ability of no correlation (P) and the slope of the log–log trait relation (α) are reported. Data sources are described in the text.

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2010 and Zhou et al. 2014a). This approach is clearly approxi-mated, but should offer a reasonable estimate of the trends in Vc,max′ during drying. The declines of Vc,max′ and measured stomatal conductance were then fitted by the Weibull function of leaf water potential to obtain ψ50,M and ψ50,S, respectively. For consistency, pre-dawn water potential levels reported by Zhou et al. (2014b) were converted to midday water poten-tial using species- or genus-specific relations (Martínez-Vilalta et al. 2014). The ψ50,S and ψ50,X in Figure 1c are obtained from an existing dataset (Manzoni et al. 2014b) and combining the ψ50,S values from Figure 1a with available ψ50,X for the same species from published sources (Manzoni et al. 2013a); data in Figure 1b are obtained from the other panels.

All bivariate plots in Figure 1 show relatively strong (R > 0.4) and statistically significant (P < 0.05) correlations, indicating that the water potential levels at 50% decline of metabolic capacity and hydraulic and stomatal function are coordinated across spe-cies from a range of climatic conditions. Notably, the scaling of ψ50,M and ψ50,S has a slope near one, indicating a nearly linear relation (Figure 1a). The intercept of the relation is small but positive, indicating that metabolic impairment follows stomatal closure, consistent with previous reports (Flexas et al. 2004, Galmes et al. 2007, Lawlor and Tezara 2009). It is possible that maintaining photosynthetic capacity and mesophyll conductance at much lower leaf water potential than at stomatal closure may be counterproductive, leading to the tight relation between ψ50,M and ψ50,S. In contrast, the scalings between ψ50,X and ψ50,M (Figure 1b) and between ψ50,X and ψ50,S (Figure 1c) have less than one exponent, indicating that decreasing ψ50,X and moving towards more drought-resistant species correspond to proportionally slower decline of ψ50,S and ψ50,M. Additionally, the ψ50,X is consistently lower than the water potential at 50% stomatal closure (Cruiziat et al. 2002, Brodribb et al. 2003). This pattern makes it possible for trees to avoid catastrophic hydraulic failure (Manzoni et al. 2014a) and is consistent with the long-term maximization of soil water use (Manzoni et al. 2014b).

Figure 1 illustrates trait coordination well, but should be interpreted with caution, since trait values for the same spe-cies were in some cases obtained from different studies where conditions might have been different (there are no studies simultaneously measuring the trends in hydraulic (xylem and stomatal) conductances, mesophyll conductance and photo-synthetic capacity during drought). Also, due to data limitations, only the apparent Vc,max′ could be calculated for most studies, without distinguishing between the actual metabolic limita-tions and mesophyll diffusion limitation. Moreover, changes in leaf and sapwood areas and vapor pressure deficit might alter the balance of water supply and demand, thereby changing leaf water potential and contributing to the inter-specific vari-ability in Figure 1. Finally, the steepness of the trait decline around ψ50 (not assessed here) would provide a further axis of co-variation (Zhou et al. 2014b).

Similar to the leaf economy spectrum, in the drought-response spectrum illustrated in Figure 1 trait values from species grow-ing in contrasting climates also overlap significantly. For exam-ple, a wide range of ψ50,X and ψ50,S have been observed across species in the same ecosystem (e.g., Zweifel et al. 2009, Miranda et al. 2010). Nevertheless, there is a tendency for more negative ψ50,X, ψ50,S and ψ50,M in more arid ecosystems and in conifers compared with angiosperms (Choat et al. 2012, Manzoni et al. 2013b, 2014b, Zhou et al. 2014a, 2014b). This overlap across ecosystems suggests that tradeoffs among traits allow different trait combinations that provide a similar function (e.g., transpiration rate, Manzoni et al. 2013a). In turn, this trait variability within communities explains the coexistence of spe-cies with contrasting strategies (Rodriguez-Iturbe et al. 2001, Manzoni et al. 2014b, Reich 2014).

To conclude, Zhou et al. (2014b) provide evidence of coor-dinated stomatal regulation, mesophyll conductance and photo-synthetic capacity during drought across species from different ecosystems. This type of study (especially when extended to wood hydraulic properties) allows testing the existence of drought-response trait spectra (Figure 1). Strong correlations in turn may help develop ecosystem models based on minimal parameteriza-tions of eco-physiological and abiotic processes along the soil–leaf hydraulic continuum and the atmosphere–mesophyll pathway (e.g., Vico and Porporato 2008, Egea et al. 2011, Zhou et al. 2014a). Perhaps most interesting from an ecological point of view, trait co-variation is suggestive of emerging optimality behav-ior (Maire et al. 2013, Manzoni et al. 2014b, Prentice et al. 2014), although a comprehensive optimality theory explaining these coordination patterns under drought is still missing.

Acknowledgments

The author thanks Shuangxi Zhou (Macquarie University) for sharing raw gas exchange and water potential data; Giulia Vico (SLU, Uppsala, Sweden), Gabriel Katul (Duke University), Belinda E. Medlyn (Macquarie University), the Editor Danielle Way and an anonymous reviewer for constructive comments.

Conflict of interest

None declared.

Funding

Partial support from National Science Foundation (FESD-1338694) is acknowledged.

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