Potassium fertilization increases water-use efficiency for stem biomass production without affecting intrinsic water-use efficiency in Eucalyptus grandis plantations
Introduction
In the future, climate changes are likely to result in a reduction in rainfall in most tropical regions where fast-growing tree plantations have been established (IPCC, 2013, Hawkins and Sutton, 2012), which will affect tree growth and patterns of water use (Wu et al., 2011). As high productivity implies high levels of water use, these planted forests are likely to be particularly affected by severe drought periods (Allen et al., 2010). Given the general increase in world demand for wood products (FAO, 2014), adaptive strategies providing both high growth potential and tolerance to water deficit are urgently needed to manage productive planted forests. Throughfall exclusion experiments using plastic panels to prevent a percentage of the total canopy throughfall from reaching the soil have been undertaken to examine the tree response to drought in temperate (e.g. Hanson et al., 2001) and tropical forests (e.g. da Costa et al., 2010). However, large-scale throughfall exclusion experiments have never been carried out in tropical planted forests to study the physiological adjustment mechanisms of trees in response to a combination of nutrient availability and water stress (Wu et al., 2011).
Tree water-use efficiency (WUE) is a critical parameter used for evaluating tree performance and exploring options for saving water (Monclus et al., 2006, Cernusak et al., 2007, King et al., 2013, Lévesque et al., 2014). Greater understanding of the mechanisms driving tree WUE is required for adapting management practices in areas subject to water shortage. Water-use efficiency is a conceptually simple parameter that, in general terms, defines the ability of the ecosystem to capture carbon and produce biomass as a function of water use. Measuring WUE is, however, methodologically challenging because this trait can be estimated in various ways and on various spatial and temporal scales (Hsiao, 1973, Binkley et al., 2004, Ripullone et al., 2004, Seibt et al., 2008). At a very short time scale, the intrinsic WUE in individual leaves (WUEi, the ratio of the net CO2 assimilation, A, to the stomatal conductance, gs) can be calculated using measurements of the instantaneous gas exchange through the leaves (Osmond et al., 1980). Leaf WUE can also be estimated at longer time scale using the isotope signature of the carbon incorporated in the leaves over their deployment (leaf δ13C, proxy of integrated CO2 assimilation over stomatal conductance), assuming a strong positive correlation between leaf δ13C and WUEi as observed in cereals (Farquhar and Richards, 1984) and trees (Ponton et al., 2002, Monclus et al., 2006, Cernusak et al., 2007). However, the time series of leaf δ13C cannot be used on its own as a reliable indicator of changes in plant WUE without independent estimates of gas exchange and environmental conditions occurring over leaf construction (Seibt et al., 2008). The phloem sap δ13C (proxy of crown CO2 assimilation over tree water use) has been used as an integrative indicator of short term changes (few last days) in WUE at canopy level (Cernusak et al., 2003, Cernusak et al., 2007, Cernusak et al., 2013, Keitel et al., 2003, Keitel et al., 2006, Merchant et al., 2010, Rascher et al., 2010). As phloem sugar concentration has been found to be closely correlated with phloem sap δ13C, phloem sugar concentration has been proposed as a reliable surrogate for phloem sap δ13C and, therefore, for WUE in eucalypt trees (Tausz et al., 2008). At stand scale, water-use efficiency for stemwood production, defined as the ratio of stemwood biomass increment to water transpired over the same period, is a highly integrative indicator taking into account all events occurring during biomass accumulation (Law et al., 2002). Because intrinsic WUE in individual leaves and WUE to produce wood may respond differently to environmental conditions (Lindroth and Cienciala, 1996, Binkley et al., 2004, Niu et al., 2011), WUE must be studied at various scales to provide more information on the sources of spatio-temporal variations.
WUE is implicitly sensitive to environmental conditions and consequently to environmental changes. Water and nutrient availability strongly affect growth as well as resource use efficiency and biomass partitioning in planted forests (Binkley et al., 2004, Stape et al., 2004, Beer et al., 2009, White et al., 2014). An increase in resource availability is likely to increase tree productivity and WUE for wood production by shifting the A:gs ratio in favor of A (increasing WUEi) and/or by shifting biomass partitioning to aboveground tree components (Litton et al., 2007, Ryan et al., 2010). Whereas a water deficit often leads to an increase in WUEi through stomatal closure (Bréda et al., 2006, Ainsworth and Long, 2005), it tends to lead to a decrease in WUE for wood production by increasing the fraction of the CO2 assimilated that is allocated to the roots (Litton and Giardina, 2008, Franklin et al., 2012). Olbrich et al. (1993) showed that large differences in WUE for wood production among four Eucalyptus grandis clones growing at the same site in South Africa were the result of differences in growth rates rather than transpiration rates. However, there are few comprehensive field studies combining measurements of WUE at different scales with different water supply regimes in tree plantations (White et al., 2009a, White et al., 2014, Albaugh et al., 2013). Ways of improving tree WUE in areas subject to water deficit must be found, which requires a quantitative understanding of the physiological responses to water stress (Dvorak, 2012, Marguerit et al., 2014). Nutrient supply may improve WUE in plants subject to water shortages (Cakmak, 2005). Potassium (K) and sodium (Na) fertilizations increased WUEi in cacao plants (Gattward et al., 2012) and olive trees (Erel et al., 2014). Although high concentrations of salt in soils significantly reduce the yields of agricultural crops (Munns, 2005), Na may replace K for various physiological functions (Wakeel et al., 2011, Kronzucker et al., 2013, Erel et al., 2015). In a E. grandis plantation on highly weathered tropical soils, K and Na supply increases tree growth, wood production, leaf gas exchange and stomatal sensitivity to water deficit of trees (Battie-Laclau et al., 2014a, Battie-Laclau et al., 2014b), and reduces the fraction of carbon allocated belowground (Epron et al., 2012). Na supply alleviates the functional and structural limitations on CO2 assimilation rates in E. grandis trees growing in K-deficient soils (Battie-Laclau et al., 2014b), as also shown recently for olive trees (Erel et al., 2014). K and Na supply might, therefore, be an appropriate means of improving WUE for wood production where there is a shortage of water. However, the effects of K and Na availability on the mechanisms controlling WUE for wood production have yet to be determined.
Within the Eucalyptus genus, the highly productive E. grandis species is most commonly planted worldwide in moist, warm subtropical regions (Harwood, 2011). This study set out to gain insights into the effects of K and Na availability on the WUE of E. grandis trees under contrasting water supply regimes. We tested the hypotheses that (1) fertilizations that increase tree growth increase WUE for stemwood production by increasing both intrinsic WUE (the ratio of the net CO2 assimilation to the stomatal conductance in individual leaves) and aboveground biomass partitioning for stemwood production, and (2) WUE at leaf and canopy levels can be predicted from leaf and phloem sap δ13C, as well as from sugar concentrations in phloem sap. However, the first hypothesis was only tested for the control treatment and K-fertilized trees as sap flow and consequently, WUE for wood production, were not measured for Na-fertilized trees.
Section snippets
Study area
The experiment was conducted at the Itatinga Experimental Station of the University of São Paulo in Brazil (23°02′S; 48°38′W). Over the previous 15 years, the mean annual rainfall was 1360 mm. The mean monthly temperature was 15 °C during the dry season from June to September, and 25 °C during the rainy season from October to May. The time series for the daily rainfall, vapor pressure deficit (VPD) and soil water content over the study period can be found in Battie-Laclau et al. (2014b).
The
Aboveground net primary production (ANPP)
Na and K fertilization increased the ANPP over the study period by a factor of 1.5 and 2.2, respectively (Fig. 1a). A significant interaction between the water supply regime and fertilization showed that applying K and Na was less effective at increasing ANPP in −W plots than in +W plots (Table 1). The effects of fertilization on the annual ANPP increased with the age of the trees (there was a significant interaction between fertilization and tree age). The effects of throughfall exclusion on
Effects of fertilization and throughfall exclusion on tree growth
K, and to a lesser extent Na supply, increased stemwood production. Previous studies in this experimental setup showed that gross primary production (GPP) was also greatly increased by K and Na fertilization as a result of lower stomatal and mesophyll resistance to CO2 diffusion and higher photosynthetic capacity in the leaves (Battie-Laclau et al., 2014a), as well as an increase in total leaf area and light use efficiency (Christina et al., 2015). K fertilization has been shown to increase
Conclusion
While different fertilization and water supply regimes had little effect on intrinsic WUE, favorable growing conditions clearly increased WUE for stemwood production. Allocation patterns in response to nutrient and water supply appeared to be a major driver of WUE for stemwood production. Consequently, leaf and phloem δ13C, which are common proxies of WUE at leaf level, were unable to predict large changes in WUE for stemwood production of our E. grandis clone. These results contribute to
Acknowledgments
We should like to thank the staff at the Itatinga Experimental Station (ESALQ-USP), in particular Rildo Moreira e Moreira (Esalq, USP), as well as Eder Araújo da Silva and FLORAGRO (www.floragroapoio.com.br) for their technical support. We acknowledge the CENA laboratory (USP, Piracicaba, Brazil) and the BPMP laboratory (INRA, Montpellier, France) for the δ13C analyses. The study was funded by FAPESP (www.fapesp.br, 2010/50663-8), CIRAD, USP-COFECUB (Project 2011-25), AGREENIUM (Plantrotem
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