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Drought effect on plant nitrogen and phosphorus: a metaanalysis Mingzhu He1* and Feike A. Dijkstra2* 1

Shapotou Desert Research and Experiment Station, Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences, Lanzhou, 730000, China;

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Department of Environmental Sciences, Centre for Carbon, Water and Food, The University of Sydney, Camden, NSW 2570, Australia

Summary Author for correspondence: Mingzhu He Tel: +86 931 4967193 Email: [email protected] Received: 13 May 2014 Accepted: 22 June 2014

New Phytologist (2014) doi: 10.1111/nph.12952

Key words: drought duration, drought manipulation type, drought stress, drying– rewetting cycle, N : P ratio, nutrient mineralization.

 Climate change scenarios forecast increased aridity in large areas worldwide with potentially important effects on nutrient availability and plant growth. Plant nitrogen and phosphorus concentrations (plant [N] and [P]) have been used to assess nutrient limitation, but a comprehensive understanding of drought stress on plant [N] and [P] remains elusive.  We conducted a meta-analysis to examine responses of plant [N] and [P] to drought manipulation treatments and duration of drought stress.  Drought stress showed negative effects on plant [N] ( 3.73%) and plant [P] ( 9.18%), and a positive effect on plant N : P (+ 6.98%). Drought stress had stronger negative effects on plant [N] and [P] in the short term (< 90 d) than in the long term (> 90 d). Drought treatments that included drying–rewetting cycles showed no effect on plant [N] and [P], while constant, prolonged, or intermittent drought stress had a negative effect on plant [P].  Our results suggest that negative effects on plant [N] and [P] are alleviated with extended duration of drought treatments and with drying–rewetting cycles. Availability of water, rather than of N and P, may be the main driver for reduced plant growth with increased long-term drought stress.

Introduction Most climate change scenarios forecast that much of the global land area will undergo increasing aridity (Handmer et al., 2012). Because nitrogen (N) and phosphorus (P) frequently limit plant growth, an improved understanding of the N and P cycles within the soil–plant system in response to drought stress is becoming increasingly important. From a global point of view, drought (simply defined as water deficit in soil and/or atmosphere) affects plant survival (Bray, 1997), ecosystem production (Farooq et al., 2012) and function (Ledger et al., 2013). Water availability is a key driver of ecosystem processes, therefore drought stress will probably alter ecosystem N and P cycles (Sardans & Pe~ nuelas, 2012). Plant N and P concentrations (hereafter plant [N] and [P]) are important indicators of N and P limitation (Aerts & Chapin, 2000; G€ usewell, 2004), but impacts of drought on plant [N] and [P] remain unclear. Drought can depress plant growth by reducing N and P uptake, transport and redistribution (Rouphael et al., 2012). A majority of studies have indicated that plants decrease N and P uptake with a decline in soil moisture (Cramer et al., 2009; Waraich et al., 2011; Sardans & Pe~ nuelas, 2012). Owing to a reduction in *These authors contributed equally to this work. Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

stomatal conductance, photosynthesis and transpiration rates also decrease, and CO2 assimilation rates progressively decline in response to drought (Farooq et al., 2012). Therefore, drought effects on plant [N] and [P] may depend on the reduction in N and P uptake relative to the decrease in CO2 assimilation. Drought stress and associated reduction in soil moisture can reduce plant nutrient uptake by reducing nutrient supply through mineralization (Fierer & Schimel, 2002; Schimel et al., 2007; Sanaullah et al., 2012), but also by reducing nutrient diffusion and mass flow in the soil (Chapin, 1991; Lambers et al., 2008). When drought stress is followed by rewetting, this often results in enhanced mineralization (Austin et al., 2004), which has been attributed to nutrient release from dead microbial biomass that has accumulated during the drying period (Borken & Matzner, 2009). The net effect of drought stress on nutrient supply through mineralization may depend on the duration and intensity (or severity) of these drying–rewetting cycles, which can be attributed to many factors, such as frequency and occurrence of rainfall, soil type affecting water potential, and evapotranspiration demand (Farooq et al., 2009). Generally, negative effects on soil microbial activity and plant nutrient uptake become larger with increased drought stress, but frequent rewetting events after drought periods may, at least in part, compensate for the negative effects of New Phytologist (2014) 1 www.newphytologist.com

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drought on nutrient supply and plant uptake (Austin et al., 2004; Borken & Matzner, 2009). Recently it was shown that with increased aridity the N and P cycle may become decoupled with reduced N concentrations and increased P concentrations in the soil (Delgado-Baquerizo et al., 2013). However, it is unclear how plant N : P ratios respond to drought (Sardans et al., 2008; Sardans & Pe~ nuelas, 2012). The diffusivity of P in the soil may be more sensitive to soil moisture than that of N (Lambers et al., 2008). Supply of P in many soils is also derived from desorption and dissolution of inorganic P, which may be sensitive to soil moisture (Belnap, 2011). Because of these differences of N and P in the soil, changes in plant [N] and [P] in response to drought may not be the same in magnitude and direction. Although effects of drought stress on plant N and P have been assessed in many field and pot studies, the results have been inconsistent. Furthermore, differences in drought stress manipulation methods, including duration and intensity of drought treatments, have muddled clear relationships between drought stress and plant [N], [P] and N : P. We conducted a meta-analysis to test if clear relationships between drought stress and plant [N] and/or [P] exist, using published studies. We hypothesized that drought stress reduces [N] and [P] in plant tissues, resulting from reduced uptake of plant nutrients and a decline in N and/or P availability in the soil. Secondly, because desorption and plant uptake of P are more sensitive to drought than mineralization and plant uptake of N, we hypothesized that the reduction of plant [P] is larger than the reduction of plant [N] with drought, resulting in increased plant N : P. Thirdly, we hypothesized that the negative effect on plant [N] and [P] will be alleviated with extended duration (from the short to the long term) of drought treatments and with drying–rewetting cycles.

Materials and Methods Data compilation We collected data from journal articles where both plant [N] and [P] were reported in response to drought. For our meta-analysis we searched the literature by using the search terms (drought OR water stress OR rainout shelter) AND nitrogen AND phosphorus in Web of Science (ISI), Google Scholar, and Scopus. We screened publications and a total 155 observations of plant [N] and [P] (Table S1) were taken from 25 papers (Supporting Information, Notes S1). The following criteria were adopted to choose appropriate studies:  N and P concentrations in green foliage or above-ground biomass in drought stress (DS) treatments and control treatment had to be reported.  The DS and control treatment started with the same soil type and plant species, and were conducted under equal spatial and temporal scales.  DS in the studies was implemented either by using rainout shelters in the field or by manipulating soil water content (SWC) in controlled-environment facilities (pot experiments). Under the DS treatments, all studies had a water deficit in soils compared New Phytologist (2014) www.newphytologist.com

with the control treatments. Therefore, field studies where SWC was increased with irrigation were not included.  Drought manipulation method, duration, and/or frequency of drought had to be reported. When studies included other treatments (e.g. plant species, atmospheric CO2, temperature, fertilization), they were used as separate observations. Several studies also reported plant [N] and [P] at multiple times. Because we were interested in how plant [N] and [P] varied with time, each measurement in time was treated as a separate observation. For each publication, we noted the location, drought manipulation method, plant species and functional group, treatment duration, and the response variables. We also collected above-ground biomass and the extractable soil N (sum of NH4+ and NO3 ) or P in control and DS treatments when reported (Table S2). Extractable soil N was determined by 2 M KCl extraction, and extractable soil P was measured by NaHCO3 extracts of the Olsen method (Watanabe & Olsen, 1965). Data in the original paper’s figures were extracted by Getdata Graph Digitizer (version 2.22; http:// getdata-graph-digitizer.com). We calculated the standard deviation from sampling size and standard error if not reported. Drought stress in the field and pot experiments was implemented using different timescales (from 1 d to several years) and frequency. We focused our meta-analysis on the temporal SWC conditions caused by DS manipulation type and its duration. We grouped our data according to DS manipulation into four types (Fig. 1): constant-stressed type – the control and DS treatment were kept at a constant SWC throughout the duration of the experiment (with lower SWC for the DS treatment, type I); drying and rewetting cycling type – both control and DS treatments underwent drying–rewetting cycles, but the drying–rewetting cycle for the DS treatment had overall lower SWC (type II); prolonged drying type – both the control and DS treatments started at the same SWC, but the control treatment was held at constant SWC and the DS treatment decreased in SWC with time (type III); and intermittent drying type – the SWC in the DS treatment was the same as in the control treatment or at a lower level, but with a reduction in SWC during a specific growth stage period (type IV). Duration of DS treatment was grouped into three categories: short-term treatment (0–30 d), medium-term treatment (31–90 d) and long-term treatment (> 90 d). Statistical analyses For plant and soil parameters, we used the natural log of the response ratio as a metric of the effect size in the meta-analysis, loge R = loge (Xd/Xc), where Xd and Xc are the mean values for the drought stress and control treatments, respectively. A value of logeR = 0 indicates that the DS treatment had no effect. The variance of logeR for each study was calculated using the inverse of the pooled variance (Hedges & Olkin, 1985; Hedges et al., 1999). In a few studies where the standard deviations (SDs) were not reported, we approximated the missing SD by multiplying the reported mean by the average coefficient of variance (CV) of our complete dataset (Bai et al., 2013). We calculated mean effect Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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Fig. 1 Drought stress (DS) manipulation types used in the meta-analysis. We classified DS manipulation treatments into the following four types: (a) type I, constantstressed type – soil water content (SWC) in control and DS treatments is constant throughout the experiment with lower SWC in the DS treatment (n = 59); (b) type II, drying–rewetting cycle type – control and DS treatments have identical frequency of drying–rewetting cycles; however, the SWC content in the DS treatment was lower overall (n = 11); (c) type III, prolonged drying type – the DS treatment started with the same SWC as the control, but the SWC gradually decreased until termination of the experiment (n = 30); and (d) type IV, intermittent drying type – the SWC in the DS treatment was the same as in the control treatment or at a lower level, but with a reduction in SWC during a specific growth stage period (n = 55).

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sizes and generated 95% confidence intervals (CIs) using the random-effects model in MetaWin 2.1 (Rosenberg, 2000). For bootstrapping we used 4999 iterations. Drought stress treatments were considered significant if the 95% CI did not overlap with zero. The logeR mean effect sizes were back-transformed and DS effects were reported as a percentage change compared with controls (100(R 1)). The use of more than one observation within a study may have overrepresented an effect from studies with a large number of observations. To test if this was the case, we randomly chose one observation from each study and conducted the same analysis for those selected observations only. A mean effect size calculated for this selected dataset similar to the mean effect size of the whole dataset suggests that overrepresentation of effects from particular studies did not occur (Garcıa-Palacios et al., 2013). We evaluated if effects differed among DS manipulation types (types I–IV), duration categories of DS (short term, medium term, long term), functional group type (tree, shrub, grass), N fixation (nonfixing, N-fixing), and experiment type (field experiment, pot experiment) using the Q between statistics. Differences between categories were considered significant when Prandom < 0.05. Relationships between effect sizes of plant [N], [P] and N : P and effect sizes of above-ground biomass were determined using linear regressions (using JMP, version 10, SAS Institute, Cary, NC, USA).

Results Plant [N], [P] and N : P showed different responses to drought stress across all observations. The overall effect of DS on plant [N] and [P] was negative, with average decreases of 3.73 and 9.18%, respectively (Fig. 2a,b), while the effect on plant N : P was positive, with an increase of 6.98% (Fig. 2c). Effect sizes and their 95% CIs did not overlap with zero, indicating significant DS effects (Fig. 2d). Mean effect sizes were similar when we used Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

one observation for each study (Table S3), suggesting that mean effect sizes were not overrepresented by studies with a large number of observations. Drought stress had different effects on soil inorganic N and P. Soil extractable N (sum of NH4+ and NO3 ) responded positively to DS and increased, on average, by 11.7% (Fig. 3). By contrast, DS significantly decreased extractable P (mean effect size = 83.7%; Fig. 4). The effect on extractable soil N : P was not significant. We note that there were only five observations for extractable P and N : P. We grouped DS manipulation into four types (Figs 1, 4) and duration of DS into three categories (Fig. 4). Plant [N], [P] and N: P had different responses to DS manipulation types and duration. Plant [N] was not significantly different among the four types of DS manipulation (Qbetween = 4.56, df = 3, Prandom = 0.23). Only in the type I manipulation (constant-stressed) was the mean effect size significantly lower than zero (decreases of 4.82%; Fig. 4a). The duration of treatment showed a significant effect on plant [N] (Qbetween = 14.1, df = 2, Prandom = 0.001). The mean effect size for plant [N] decreased the most in the short-term treatment (average decrease of 10.2%) and disappeared in the long-term treatment (Fig. 4a). Plant [N] decreased more in field than in pot experiments and more in nonfixing plants than in N-fixing plants (Table S4). Plant [P] showed significantly different responses to the DS manipulation types (Qbetween = 13.1, df = 3, Prandom = 0.02). While type I, type III, and type IV had negative effects on plant [P] (decreases of 7.61, 17.25 and 9.65%, respectively), type II had no effect on plant [P] (Fig. 4b). As with plant [N], the duration of DS had a significant effect on plant [P] (Qbetween = 13.7, df = 2, Prandom = 0.005). Decreases in plant [P] in response to DS were strongest in the short term (average decrease of 18.1%) and smallest in the long term (average decrease of 0.68%; Fig. 4b). Plant [P] was not affected by functional group type or experiment type (Table S4). New Phytologist (2014) www.newphytologist.com

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Fig. 2 The frequency distribution of the effect size (natural log of the response ratio, logeR) for plant [N] (a), plant [P] (b), plant N : P (c) to drought stress, and mean effect sizes of drought stress treatment on plant [N], [P] and N : P (d). The solid curve in (a–c) is a Gaussian distribution fitted to the frequency data (n, the number of observations). The error bars in (d) represent 95% bootstrapped confidence intervals (CIs). The effect of drought stress was considered significant if the 95% CI of logeR did not overlap with zero.

significantly greater than zero (average increase of 16.0%; Fig. 4c). There was no significant response of plant N : P to duration of DS (Qbetween = 5.88, df = 2, Prandom = 0.11). However, the mean effect size of plant N : P was significantly larger than zero in the short term (average increase of 12.5%), and this positive effect of DS decreased to 3.16% in the long term (Fig. 4c). Plant N : P increased more in pot than in field experiments, but was not affected by functional group type (Table S4). The effect size (logeR) of plant [N] was negatively related to the effect size of above-ground biomass (r2 = 0.46, P = 0.019; Fig. 5a). Similarly, logeR of leaf [P] also showed a negative relationship with logeR of above-ground biomass (r2 = 0.29, P = 0.049; Fig. 5b). There was no relationship between logeR of plant N : P and above-ground biomass (Fig. 5c). Fig. 3 Meta-analysis results of the responses of soil extractable nitrogen (N), phosphorus (P) and N : P to drought. Error bars represent 95% bootstrapped confidence intervals (CIs). The effect of drought stress was considered significant if the 95% CI of the mean effect size did not overlap with zero. The number of observations for each category is shown in brackets.

Plant N : P showed no significant differences among the four DS types (Qbetween = 5.88, df = 3, Prandom = 0.11). The mean effect size of plant N: P for the type III manipulation was New Phytologist (2014) www.newphytologist.com

Discussion Our meta-analysis supported our first two hypotheses. Across all 155 observations, DS had negative effects on plant [N] and plant [P], with a larger decrease for plant [P] than for plant [N]. Our results suggest that across all observations the reduction in N and P uptake was larger than the reduction in plant growth, so that plant [N] and [P] declined with DS. However, there was Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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Fig. 4 The mean effect sizes of drought on plant nitrogen (N) (a), plant phosphorus (P) (b), and plant N : P (c) categorized by drought stress (DS) manipulation type and duration. Type I, constant-stressed type; type II, drying and rewetting cycling type; type III, prolonged drying type; type IV, intermittent drying type; short term, < 30 d; medium term, between 31 and 90 d; long term, > 90 d. Error bars represent 95% bootstrapped confidence intervals (CIs). The effect of drought stress was considered significant if the 95% CI of the effect size did not overlap with zero. The number of observations for each category is shown next to the error bars. Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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considerable variability in plant [N] and [P] responses to DS. Decreases were observed in constant-stressed (plant [N] and [P]), prolonged drying (plant [P]), and intermittent drying treatment types (plant [P]), and most strongly in short-term observations. On the other hand, plant [N] and [P] were not affected by the drying–rewetting treatment type and in long-term observations. Drying–rewetting can increase soil N availability after rewetting, partly or completely compensating for the reduced N mineralization during the drying period (Borken & Matzner, 2009). A rapid increase of soil water potential after rewetting can lead to microbial osmotic shock, including microbial cell lysis (Bottner, 1985; Van Gestel et al., 1993), release of intracellular solutes (Halverson et al., 2000), and enhanced decomposition of dead microbial biomass (Bottner, 1985). The increase in decomposition of organic matter after rewetting may also increase gross and net N mineralization (Peterjohn & Schlesinger, 1990; Mummey et al., 1994). An increase in soil available N after rewetting may explain why plant [N] was not affected by DS in the drying– rewetting treatment type. Drying–rewetting also had no significant effect on plant [P] (Fig. 4b). More than 90 yr ago, Lebedjantzev (1924) found a substantial release of P as a result of drying and moistening of a soil. In a grassland soil, water-soluble P increased as a consequence of drying–rewetting cycles and it was argued that this increase in P had a microbial source and was mainly caused by osmotic shock and cell lysis (Turner & Haygarth, 2001). As with N, this increase in soil available P after rewetting may have compensated for the reduced P availability during the drying period so that plant [P] remained unaffected. We found that DS caused short-term decreases in plant [N] and plant [P], but that these effects disappeared in the long term (> 90 d), supporting our third hypothesis. Short-term drought conditions appeared to have reduced N and P uptake more than C assimilation, while in the long term, the negative effects on plant [N] or [P] were alleviated. A reduction in soil moisture with short-term DS may reduce microbial activity and net N mineralization (Borken & Matzner, 2009). A reduction in soil moisture may also reduce nutrient diffusivity and mass flow (Rouphael et al., 2012). Both of these soil moisture effects may reduce plant N and P uptake in the short term, more so than C assimilation. With time, plants may adjust their growth, morphology, and physiochemical characteristics to adapt to drought stress. Enhanced root growth and extension may absorb more water and nutrients (N and P, etc.) from deeper soils (Subbarao et al., 1995; Turner & Haygarth, 2001). Nutrient uptake under DS could be further enhanced by increasing the root : shoot ratio in DS environments (Chapin et al., 1993). Drying–rewetting cycles are also likely to occur more frequently with increased time, which may have improved N and P supply further under drought conditions. Unfortunately, with our data set, we were unable to separate duration effects from manipulation type effects. Because pot experiments tend to be shorter in duration than field experiments, the duration effect may also have been influenced by experiment type. However, we found no evidence that plant [N] and [P] decreased more in pot than in field experiments in New Phytologist (2014) www.newphytologist.com

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Fig. 5 Relationships of the effect size (natural log of the response ratio, logeR) of plant [N] (a), plant [P] (b), and plant N : P (c) with effect sizes of plant above-ground biomass (logeR of above-ground biomass). Significant relationships were found in (a) and (b) (P < 0.05); there was no significant relationship in (c) (P > 0.05).

response to DS (Table S4). In fact, plant [N] was reduced more in field than in pot experiments. Regardless, our results suggest that plants under drought stress lasting longer than 90 d may have adapted to the new conditions and established a new equilibrium between plant growth and plant N and P uptake so that plant [N] and [P] were unaffected. It is possible that, under severe DS, plant growth may decrease more than plant N and P uptake. The negative relationships we (a)

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observed between effect sizes of above-ground biomass and plant [N] and [P] (Fig. 5a,b) suggest that with large reductions in plant biomass, plant [N] and [P] may actually increase in response to DS. Possibly, with less soil moisture, plants respond by growing more root biomass (and roots’ absorptive surface) relative to shoot biomass (Lambers et al., 2008), which in combination with more concentrated available forms of N and P in the soil may result in higher above-ground [N] and [P] under severe DS.

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Fig. 6 A conceptual framework describing the responses of plant [N] and [P], soil extractable N and P to drought stress (DS). (a), (b) and (c) represent three pathways affecting plant [N] and [P] through changing the balance between plant carbon (C) assimilation and nutrient uptake. ↑, increase in pool sizes or concentrations in response to drought stress; ↓, decrease in pool sizes or concentrations in response to drought stress; =, no effect on pool sizes or concentrations; –, negative effects on carbon and nutrient flows. The size of the negative signs indicates the strength of the effect. Green dashed block, nutrient-limited mechanisms in response to DS; red dashed block, waterlimited mechanisms in response to DS. See text for details. New Phytologist (2014) www.newphytologist.com

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New Phytologist Mycorrhizas may also play a greater role in nutrient uptake under DS conditions (Alvarez et al., 2009; Danielsen & Polle, 2014). Our meta-analysis indicates that DS had a positive effect on extractable N and a negative effect on extractable P (Fig. 3). The analysis resulted from 33 observations conducted in the field with rainout shelters controlling drought manipulation in a semiarid Patagonian steppe (Yahdjian et al., 2006), a Mediterranean mountain forest (Matıas et al., 2011) and a tropical forest (Wood & Silver, 2012). In semiarid and Mediterranean-type ecosystems, a rainfall reduction often leads to nutrient accumulation in the soil during the dry period, because of a stronger reduction in plant uptake compared with mineralization rates in the soil (Kozlowski & Pallardy, 2002; Matıas et al., 2011). In a humid tropical forest, Wood & Silver (2012) indicated that drought was likely to improve the soil redox potential so that more iron oxide and hydroxide minerals would bind with P, thereby removing P from the soil exchange complex, which leads to P limitation in the soil–plant system. Therefore, changes in soil available N and P in response to DS treatment may be ecosystem-specific. Our results should be treated with caution because they came from a small number of studies, taken at specific points in time (thereby potentially missing important changes in soil nutrient availability), and from specific ecosystems. Our results are also in contrast to a study across 224 dryland sites where total soil N concentrations decreased, but total soil P concentrations increased with increased aridity (Delgado-Baquerizo et al., 2013). Based on our results, we present a conceptual framework to interpret the possible mechanisms of how DS may affect plant [N] and [P] (Fig. 6). The first pathway (Fig. 6a) considers the decrease of plant N and P uptake resulting from a reduction in soil moisture and soil nutrient mineralization, thereby reducing available pools of N and P in the soil. In this scenario, DS may decrease C assimilation also, but when plant growth is limited by N and/or P, reduced N and P availability will result in lower plant [N] and/or [P]. This first pathway may occur in nutrientpoor environments, where plant growth is not limited by water availability for most of the year. Secondly, drought conditions may decrease mass flow or diffusivity of nutrients, thereby restricting nutrient transport between roots and shoots, and thus N and P uptake. This negative effect on nutrient transport would be stronger for P than for N, because diffusivity of P in the soil is more sensitive to soil moisture than that of N (Lambers et al., 2008). A reduction in plant nutrient uptake without a change in mineralization or microbial uptake may then cause accumulation of inorganic N and P in the soil (Fig. 6b). Nitrogen may accumulate more than P because of the potential increase in P fixation with drier soil conditions (Wood & Silver, 2012). Despite the increase in soil N and P that is potentially available to plants, plants are not able to take up these nutrients because of limited water availability. In this scenario, plant [N] and [P] would decrease when plant growth is limited by nutrients and water supply. The effect of DS through the second pathway may be short-lived if, with time, plants are able to adapt to the new drought conditions (Subbarao et al., 1995; Rouphael et al., 2012). The third pathway (Fig. 6c) illustrates plant adaptation to long-term drought stress. Photosynthesis and transpiration Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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decrease as a result of reduced stomatal conductance and carbon (C) assimilation, leading to a reduction in shoot biomass, while plants may spend relatively more C assimilates on root growth to improve water and nutrient uptake under drought conditions. Drying–rewetting events may also occur more often in the long term, which could improve N and P supply to plants through mineraliszation under increased DS. As a result, the reduction in plant growth and plant nutrient uptake may become more balanced in the long term, causing no effect on plant [N] and [P] (or with severe DS, plant [N] and [P] may even increase). We expect this last pathway to occur particularly in semiarid and arid environments where water availability is limiting plant growth during most of the year. Conclusions Plant [N] and [P] have been used to indicate if plant growth is limited by N and/or P (Aerts & Chapin, 2000). Our meta-analysis has indicated that drought stress generally decreased plant [N] and [P], but increased plant N : P. The increase in soil available N and decrease in soil available P may have contributed to the increase in plant N : P in response to DS, but our number of soil observations was limited. Our results suggest that DS may enhance N and P limitation on plant growth (P more than N), but that these effects are only transient. Plant growth may not become more limited by N and P with increased long-term DS; instead, water availability may become the main driver for reduced plant growth with increased long-term DS.

Acknowledgements We are grateful to Dr Amy Austin and three anonymous referees for feedback on an earlier draft. We also thank the authors whose work was included in this meta-analysis. This work was supported by the Australian Research Council (FT100100779) and the National Science Foundation of China (grant no. 41101054).

References Aerts R, Chapin FS. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. In: Fitter AH, Raffaelli DG, eds. Advances in ecological research, vol 30. San Diego, CA, USA: Elsevier Academic Press Inc., 1–67. Alvarez M, Huygens D, Olivares E, Saavedra I, Alberdi M, Valenzuela E. 2009. Ectomycorrhizal fungi enhance nitrogen and phosphorus nutrition of Nothofagus dombeyi under drought conditions by regulating assimilative enzyme activities. Physiologia Plantarum 136: 426–436. Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM. 2004. Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141: 221–235. Bai E, Li SL, Xu WH, Li W, Dai WW, Jiang P. 2013. A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. New Phytologist 199: 441–451. Belnap J. 2011. Biological Phosphorus Cycling in Dryland Regions. In: B€unemann EK, Oberson A, Frossard E, eds. Phosphorus in action. Berlin, Heidelberg, Germany: Springer, 371–406. Borken W, Matzner E. 2009. Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Global Change Biology 15: 808–824. New Phytologist (2014) www.newphytologist.com

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8 Research Bottner P. 1985. Response of microbial biomass to alternate moist and dry conditions in a soil incubated with 14C- and 15N- Labeled plant-material. Soil Biology & Biochemistry 17: 329–337. Bray EA. 1997. Plant responses to water deficit. Trends in Plant Science 2: 48–54. Chapin FS III. 1991. Effects of multiple environmental stresses on nutrient availability and use. In: Mooney HA, Winner WE, Pell EJ, eds. Response of plants to multiple stresses. San Diego, CA, USA: Academic Press, 67–88. Chapin FS III, Autumn K, Pugnaire F. 1993. Evolution of suites of traits in response to environmental-stress. American Naturalist 142: S78–S92. Cramer MD, Hawkins HJ, Verboom GA. 2009. The importance of nutritional regulation of plant water flux. Oecologia 161: 15–24. Danielsen L, Polle A. 2014. Poplar nutrition under drought as affected by ectomycorrhizal colonization. Environmental and Experimental Botany, in press. doi: 10.1016/j.envexpbot.2014.01.006. Delgado-Baquerizo M, Maestre FT, Gallardol A, Bowker MA, Wallenstein MD, Quero JL, Ochoa V, Gozalo B, Garcıa-Gomez M, Soliveres S et al. 2013. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502: 672–676. Farooq M, Hussain M, Wahid A, Siddique KHM. 2012. Drought stress in plants: an overview. In: Aroca R, ed. Plant responses to drought stress. Berlin, Heidelberg, Germany: Springer, 1–33. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA. 2009. Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development 29: 185–212. Fierer N, Schimel JP. 2002. Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biology & Biochemistry 34: 777–787. Garcıa-Palacios P, Maestre FT, Kattge J, Wall DH. 2013. Climate and litter quality differently modulate the effects of soil fauna on litter decomposition across biomes. Ecology Letters 16: 1045–1053. G€ usewell S. 2004. N: P ratios in terrestrial plants: variation and functional significance. New Phytologist 164: 243–266. Halverson LJ, Jones TM, Firestone MK. 2000. Release of intracellular solutes by four soil bacteria exposed to dilution stress. Soil Science Society of America Journal 64: 1630–1637. Handmer J, Honda Y, Kundzewicz ZW, Arnell N, Benito G, Hatfield J, Mohammad A, Peduzzi P, Wu S, Sherstyukov B et al. 2012. Managing the risks of extreme events and disasters to advance climate change adaptation. In: Field CB, Barros V, Stocker TF, Qin D, Dokken DJ, Ebi KL, Mastrandrea MD, Mach KJ, Plattner G-K, Allen SK, Tignor M, Midgley PM, eds. A special report of Working Groups I and II of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press. Hedges LV, Gurevitch J, Curtis PS. 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80: 1150–1156. Hedges LV, Olkin I. 1985. Statistical methods for meta-analysis. Orlando, FL, USA: Academic Press. Kozlowski TT, Pallardy SG. 2002. Acclimation and adaptive responses of woody plants to environmental stresses. Botanical Review 68: 270–334. Lambers H, Chapin FS, Pons TL. 2008. Plant physiological ecology. New York, NY, USA: Springer. Lebedjantzev AN. 1924. Drying of soil, as one of the natural factors in maintaining soil fertility. Soil Science 18: 419–447. Ledger ME, Brown LE, Edwards FK, Milner AM, Woodward G. 2013. Drought alters the structure and functioning of complex food webs. Nature Climate Change 3: 223–227. Matıas L, Castro J, Zamora R. 2011. Soil-nutrient availability under a global-change scenario in a Mediterranean mountain ecosystem. Global Change Biology 17: 1646–1657. Mummey DL, Smith JL, Bolton H. 1994. Nitrous oxide flux from a shrub steppe ecosystem: sources and regulation. Soil Biology & Biochemistry 26: 279– 286. Peterjohn WT, Schlesinger WH. 1990. Nitrogen loss from deserts in the southwestern United States. Biogeochemistry 10: 67–79. Rosenberg MS 2000. MetaWin statistical software for meta-analysis. Sunderland, MA, USA: Sinauer Associates, 1 CD-ROM.

New Phytologist (2014) www.newphytologist.com

Rouphael Y, Cardarelli M, Schwarz D, Franken P, Colla G. 2012. Effects of drought on nutrient uptake and assimilation in vegetable crops. In: Aroca R, ed. Plant responses to drought stress. Berlin, Heidelberg, Germany: Springer, 171–195. Sanaullah M, Rumpel C, Charrier X, Chabbi A. 2012. How does drought stress influence the decomposition of plant litter with contrasting quality in a grassland ecosystem? Plant and Soil 352: 277–288. Sardans J, Pe~ nuelas J. 2012. The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiology 160: 1741–1761. Sardans J, Pe~ nuelas J, Ogaya R. 2008. Drought-induced changes in C and N stoichiometry in a Quercus ilex Mediterranean forest. Forest Science 54: 513– 522. Schimel J, Balser TC, Wallenstein M. 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88: 1386–1394. Subbarao GV, Johansen C, Slinkard AE, Rao RCN, Saxena NP, Chauhan YS. 1995. Strategies for improving drought resistance in grain legumes. Critical Reviews in Plant Sciences 14: 469–523. Turner BL, Haygarth PM. 2001. Biogeochemistry: phosphorus solubilization in rewetted soils. Nature 411: 258–258. Van Gestel M, Merckx R, Vlassak K. 1993. Microbial biomass responses to soil drying and rewetting: the fate of fast- and slow-growing microorganisms in soils from different climates. Soil Biology & Biochemistry 25: 109–123. Waraich EA, Ahmad R, Saifullah, Ashraf MY, Ehsanullah. 2011. Role of mineral nutrition in alleviation of drought stress in plants. Australian Journal of Crop Science 5: 764–777. Watanabe FS, Olsen SR. 1965. Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Science Society of America Journal 29: 677–678. Wood TE, Silver WL. 2012. Strong spatial variability in trace gasdynamics following experimental drought in a humid tropical forest. Global Biogeochemical Cycles 26: GB3005. Yahdjian L, Sala O, Austin AT. 2006. Differential controls of water input on litter decomposition and nitrogen dynamics in the Patagonian steppe. Ecosystems 9: 128–141.

Supporting Information Additional supporting information may be found in the online version of this article. Table S1 Observations used in the meta-analysis for plant [N], [P] and N : P Table S2 Observations used in the meta-analysis for soil available N and P Table S3 Summary of results from the meta-analysis on plant [N], [P] and N : P – comparison of complete dataset with one random observation per study Table S4 Summary of results from the meta-analyses on plant [N], [P] and N : P – comparison of functional group and experiment type Notes S1 References used in meta-analysis. Please note: Wiley Blackwell are not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

Drought effect on plant nitrogen and phosphorus: a meta-analysis.

Climate change scenarios forecast increased aridity in large areas worldwide with potentially important effects on nutrient availability and plant gro...
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