Low acclimation potential compromises the performance of water-stressed pine saplings under Mediterranean xeric conditions

We are grateful to the Centro Nacional de Recursos Genéticos Forestales “El Serranillo” (MITECO) for cultivating the plants during the nursery stage. Moreover, we want to thank two anonymous reviewers for improving the manuscript with their comments. This study was supported by the projects RESISTE ( P18-RT-1927 ) of the Consejería de Transformación Económica, Industria, Conocimiento y Universidades from the Junta de Andalucía, and PID2019-107382RB-I00 of Ministerio de Ciencia e Innovación from Gobierno de España. Funding for open access charge: Universidad de Granada / CBUA .Predicted hotter and drier climatic conditions in the Mediterranean Basin will probably hamper current afforestations and reforestations by negatively influencing tree performance. Understanding how saplings can adjust their physiology to shortages in water availability is essential to predict early-stage success of forest ecological restoration. Pines are common target species used in afforestations and reforestations; however, the capacity of their saplings for physiological plasticity to promote drought tolerance remains largely unexplored. In this study, we evaluated the demographical and resource-use consequences of short-term irrigation among four pine species (Pinus halepensis, Pinus pinea, Pinus nigra and Pinus sylvestris) growing under water-limiting conditions in a common garden experiment. Summer irrigation increased the survival rate of those pines that were suffering from hydric stress under the xeric conditions of the common garden (i.e. P. pinea, P. nigra and P. sylvestris). Moreover, short-term water supplementation slightly enhanced aboveground biomass production across species. However, leaf isotopic composition and nutrient concentrations did not change after summer irrigation. Independently of water supplementation, P. halepensis was the best adapted species to water scarcity and showed the best physiological and growth performance. By contrast, P. pinea, P. nigra and P. sylvestris saplings exhibited drought-induced reductions in stomatal conductance and low water-use efficiency, nutrient deficiency, and severe N:P and N:K stoichiometric imbalances, leading to impaired growth. We conclude that the lack of physiological plasticity of water-stressed pine saplings to withstand the impacts of climate aridification will likely cause severe impairment of their nutrient status, growth and survival, with dire implications for the successful establishment of Mediterranean afforestation and reforestation programs.CBUAConsejería de Transformación Económica, Industria, Conocimiento y Universidades from the Junta de AndalucíaMinisterio de Ciencia e Innovación from Gobierno de EspañaUniversidad de GranadaJunta de Andalucía PID2019-107382RB-I0

Warming reduces both photosynthetic nutrient use efficiency and water use efficiency in Mediterranean shrubsWarming reduces nutrient use efficiency

[EN] The ratio between net photosynthetic rates and the foliar contents of essential plant macronutrients (N, P, K) is termed photosynthetic nutrient use efficiency (PNutUE). A universal trade-off exists whereby plants cannot maximize their PNutUE and their intrinsic water use efficiency (WUEi, carbon gain per unit water spent) simultaneously, because any increase in intercellular CO2 concentration (ci) through a greater stomatal opening would increase PNutE but also enhances transpiration and therefore decreases WUEi. Rising temperatures associated with climate change can result in large decreases in WUEi in semiarid shrubs through photosynthetic machinery impairment and enhanced stomatal conductance and transpiration, but we know remarkably little about the influence of warming and drought on PNutUE and its interplay with WUEi in dryland vegetation. Using a 6-year (2011–2017) manipulative field experiment, we examined the effects of warming (2.5ºC, W), rainfall reduction (30%, RR), and their combination (W+RR) on the photosynthetic use efficiency of three essential nutrients (PNUE, PPUE and PKUE) and on WUEi in three shrub species growing at two semiarid shrublands for the years 2015–2017. Across species, warming (W and W+RR) reduced PNUE by 42.9%, PPUE by 43.8% and PKUE by 41.5% on average relative to shrubs growing under ambient temperatures, whereas RR did not significantly affect their PNutUE. These drastic reductions in PNutUE with warming were mainly driven by non-stomatal and largely non-nutritional decreases in net photosynthetic rates, which were almost halved in warmed shrubs. The photosynthetic use efficiencies of N, P and K were inversely related to foliar δ13C, a proxy for time integrated WUEi, in both ambient (control and RR) and warmed (W and W+RR) shrubs, but with significantly smaller slopes and intercepts for warmed shrubs. Thus, plants achieve a smaller gain in PNutUE for any given increase in stomatal conductance (and reduction in WUEi) under warmer climatic conditions. The strong negative impact of warming on PNutE, along with the warming-induced shift in the trade-off between PNutUE and WUEi, could be indicative of an increasing inability of native plants to cope with warmer conditions, with dire implications for dryland vegetation productivity and survival under climate change.S

Chronically low nutrient concentrations in tree rings are linked to greater tree vulnerability to drought in nothofagus dombeyi

Forest dieback and mortality episodes triggered by droughts are receiving increasing atten-tion due to the projected increases in these extreme climate events. However, the role played by nutrient impairment in dieback is understudied, despite interactions among carbon-water balances and nutrition. Here, we followed a comparative analysis of long-term growth, intrinsic water-use efficiency (iWUE), oxygen isotopes (δ18O) and wood-nutrient composition patterns between living (L) and dead (D) trees of a Nothofagus dombeyi population, showing dieback in Argentina. The onset of the growth decline of D trees occurred ca. 40 years before death. These trees showed higher iWUE, pointing to higher drought stress. Their lower δ18O values, together with the uncoupling between δ18O and leaf-level processes, suggested a deeper source of water uptake for this vigor class. D trees showed a poorer nutritional status than L trees that likely amplified the dieback. This was supported by numerous positive associations of P-and K-concentrations in wood and related ratios with iWUE, δ18O and tree growth. Therefore, drought-related nutrient deterioration can significantly contribute to dieback and be an early warning signal of impending tree death.Fil: González de Andrés, Ester. Consejo Superior de Investigaciones Científicas. Instituto Pirenaico de Ecología; EspañaFil: Suarez, Maria Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; ArgentinaFil: Querejeta, José Ignacio. Consejo Superior de Investigaciones Científicas. Centro de Edafología y Biología Aplicada del Segura; EspañaFil: Camarero, J. Julio. Consejo Superior de Investigaciones Científicas. Instituto Pirenaico de Ecología; Españ

Pushing the limits of C3 intrinsic water use efficiency in Mediterranean semiarid steppes: responses of a drought‐avoider perennial grass to climate aridification

[EN] 1. Intrinsic water use efficiency (WUEi) reflects the trade-off between photo- synthetic carbon gain and water loss through stomatal conductance and is key for understanding dryland plant responses to climate change. Stipa tenacissima is a perennial tussock C3 grass with an opportunistic, drought- avoiding water use strategy that dominates arid and semiarid steppes across the western Mediterranean region. However, its ecophysiological responses to aridification and woody shrub encroachment, a major land-use change in drylands worldwide, are not well-understood. 2. We investigated the variations in leaf stable isotopes (δ18 O, δ13 C, δ15 N), nutrient concentrations (N, P, K), and culm water content and isotopic composition (δ18 O,δ2H) of paired pure-grass and shrub-encroached S. tenacissima steppes along a 350 km aridity gradient in Spain (10 sites, 160 individuals). 3. Culm water isotopes revealed that S. tenacissima is a shallow-rooted grass that depends heavily on recent rainwater for water uptake, which may render it vulnerable to increasingly irregular rainfall combined with faster topsoil drying under climate warming and aridification. With increasing aridity, S. tenacissima enhanced leaf-level WUEi through more stringent stomatal regulation of plant water flux and carbon assimilation (higher δ13C and δ18 O), reaching exceptionally high δ13C values (−23‰ to −21‰) at the most arid steppes. Foliar N concentration was remarkably low across sites regardless of woody shrub encroachment, evidencing severe water and N co-limitation of photosynthesis and productivity. Shrub encroachment decreased leaf P and K but did not affect S. tenacissima water status. Perennial grass cover decreased markedly with both declining winter rainfall and shrub encroachment suggesting population-level rather than individual-level responses of S. tenacissima to these changes.4. The fundamental physiological constraints of photosynthetic C3 metabolism com-bined with low foliar N content may hamper the ability of S. tenacissima and other drought-avoider species with shallow roots to achieve further adaptive improve-ments in WUEi under increasing climatic stress. A drought-avoiding water use strategy based on early stomatal closure and photosynthesis suppression during prolonged rainless periods may thus compromise the capacity of semiarid S. tena-cissima steppes to maintain perennial grass cover, sustain productivity and cope with ongoing climate aridification at the drier parts of their current distributionSISpanish Ministry of Science and Innovation, Grant/Award Number: EUR2022-134048, PRX19/00301, PID2019-107382RB-I00, CGL2013- 48753-R, CGL2010-21064, AGL- 2006-11234, PID2020-113021RA-I00, RTI2018- 098895-A-100 and RYC- 2016-20604; Fundación BBVA, Grant/ Award Number: BIOCON06/105; Universidad Rey Juan Carlos, Grant/Award Number: URJC-RNT- 063-2; European Research Council, Grant/Award Number: 647038; Generalitat Valenciana, Grant/ Award Number: CIDEGENT/2018/041; National Natural Science Foundation of China, Grant/Award Number: 41801091; China Postdoctoral Science Foundation, Grant/Award Number: 2018M643542 and 2019T120868; Fundación Séneca, Grant/ Award Number: 20654/JLI/

The Economics Spectrum Drives Root Trait Strategies in Mediterranean Vegetation

[EN] Extensive research efforts are devoted to understand fine root trait variation and to confirm the existence of a belowground root economics spectrum (RES) from acquisitive to conservative root strategies that is analogous to the leaf economics spectrum (LES). The economics spectrum implies a trade-off between maximizing resource acquisition and productivity or maximizing resource conservation and longevity; however, this theoretical framework still remains controversial for roots. We compiled a database of 320 Mediterranean woody and herbaceous species to critically assess if the classic economics spectrum theory can be broadly extended to roots. Fine roots displayed a wide diversity of forms and properties in Mediterranean vegetation, resulting in a multidimensional trait space. The main trend of variation in this multidimensional root space is analogous to the main axis of LES, while the second trend of variation is partially determined by an anatomical trade-off between tissue density and diameter. Specific root area (SRA) is the main trait explaining species distribution along the RES, regardless of the selected traits. We advocate for the need to unify and standardize the criteria and approaches used within the economics framework between leaves and roots, for the sake of theoretical consistency.S

Efectos del tratamiento combinado de suelo y planta sobre una repoblacion con pinus halepensis mill. en ambiente semiárido / José Ignacio Querejeta Mercader ; Antonio Roldán Garrigos, Víctor M. Castillo Sánchez.

Tesis-Universidad de Murcia.Consulte la tesis en: BCA. GENERAL. ARCHIVO UNIVERSITARIO. D 540.Consulte la tesis en: BCA. GENERAL. ARCHIVO UNIVERSITARIO. T.M.-1713

Topographic position modulates the mycorrhizal response of oak trees to interannual rainfall variability

Copyright by the Ecological Society of AmericaCalifornia coast live oak (Quercus agrifolia) forms tripartite symbiotic associations with arbuscular (AMF) and ectomycorrhizal (EMF) fungi. We selected oak individuals differing in topographic position and depth to groundwater (mesic valley vs. xeric hill sites) to investigate changes of tree mycorrhizal status in response to interannual rainfall variability. EMF root colonization, as well as hyphal abundance and viability in upper rhizosphere soil (0–30 cm), were negatively affected by severe multi-year drought, although not to the same extent in each topographic location. Oak trees growing in hill sites showed EMF colonization levels 19%) in upper roots during drought. EMF root colonization increased sharply at both topographic positions during the ensuing wet year (78% in valley, 49% in hill), which indicates that the mycorrhizal status of roots in upper rhizosphere soil is highly responsive to interannual rainfall variability. Across sites and years, percentage EMF colonization and soil hyphal density and viability were strongly positively correlated with soil moisture potential, but percentage AMF root colonization was not. Interestingly, changes in percentage EMF root colonization and density of viable hyphae between a wet and a dry year were proportionally much greater in xeric hill sites than in mesic valley sites. The mycorrhizal status of oak trees was particularly responsive to changes in soil moisture at the hill sites, where roots in upper rhizosphere soil shifted from almost exclusively AMF during severe drought to predominantly EMF during the ensuing wet year. By contrast, the mycorrhizal status of oaks in the valley sites was less strongly coupled to current meteorological conditions, as roots in upper soil layers remained predominantly EMF during both a dry and a wet year. Canopy shading and hydraulic lift by oaks in valley sites likely contributed to maintain the integrity and viability of EMF roots and extraradical hyphae in upper rhizosphere soil during extended drought. Our results suggest that oak woodlands in water-limited ecosystems may become increasingly reliant on the AMF symbiosis under future climate change scenarios for the U.S. southwest and other world regions.This work was supported by the National Science Foundation Biocomplexity Program (DEB 9981548) and a Fulbright postdoctoral fellowship awarded to J. I. Querejeta by the Spanish Ministerio de Educación y Ciencia (MEC). J. I. Querejeta also acknowledges support from the “Ramón y Cajal” Program of MECPeer reviewe

Bulk leaf δ18O and δ13C reflect the intensity of intraspecific competition for water in a semi-arid tussock grassland

We investigated the extent to which plant water and nutrient status are affected by intraspecific competition intensity and microsite quality in a monodominant tussock grassland. Leaf gas exchange and stable isotope measurements were used to assess the water relations of Stipa tenacissima tussocks growing along a gradient of plant cover and soil depth in a semi-arid catchment of Southeast Spain. Stomatal conductance and photosynthetic rate decreased with increasing intensity of competition during the wet growing season, leading to foliar δ18O and δ13C enrichment. A high potential for runoff interception by upslope neighbours exerted strong detrimental effects on the water and phosphorus status of downslope S. tenacissima tussocks. Foliar δ15N values became more enriched with increasing soil depth. Multiple stepwise regression showed that competition potential and/or rhizosphere soil depth accounted for large proportions of variance in foliar δ13C, δ18O and δ15N among target tussocks (57, 37 and 64%, respectively). The results presented here highlight the key role that spatial redistribution of resources (water and nutrients) by runoff plays in semi-arid ecosystems. It is concluded that combined measurement of δ13C, δ18O and nutrient concentrations in bulk leaf tissue can provide insight into the intensity of competitive interactions occurring in natural plant communities.This study was supported by the Spanish Comisión Interministerial de Ciencia y Tecnología (Grant number CGL2004-03627). J.I.Q. acknowledges financial support from the 'Ramón y Cajal' Program of the Spanish Ministerio de Educación y Ciencia and the European Social Fund.Peer reviewe

Altered leaf elemental composition with climate change is linked to reductions in photosynthesis, growth and survival in a semi‐arid shrubland

1. Climate change will increase heat and drought stress in many dryland areas, which could reduce soil nutrient availability for plants and aggravate nutrient limitation of primary productivity. Any negative impacts of climate change on foliar nutrient contents would be expected to negatively affect the photosynthetic capacity, water use efficiency and overall fitness of dryland vegetation. 2. We conducted a 4‐year manipulative experiment using open top chambers and rainout shelters to assess the impacts of warming (~2°C, W), rainfall reduction (~30%, RR) and their combination (W + RR) on the nutrient status and ecophysiological performance of six native shrub species of contrasting phylogeny in a semi‐arid ecosystem. Leaf nutrient status and gas exchange were assessed yearly, whereas biomass production and survival were measured at the end of the study. 3. Warming (W and W + RR) advanced shoot growth phenology and reduced foliar macro‐ (N, P, K) and micronutrient (Cu, Fe, Zn) concentrations (by 8%–18% and 14%–56% respectively), net photosynthetic rate (32%), above‐ground biomass production (28%–39%) and survival (23%–46%). Decreased photosynthesis and growth in W and W + RR plants were primarily linked to enhanced nutritional constraints on carbon fixation. Poor leaf nutrient status in W and W + RR plants partly decoupled carbon assimilation from water flux and led to drastic reductions in water use efficiency (WUEi; ~41%) across species. The RR treatment moderately decreased foliar macro‐ and micronutrients (6%–17%, except for Zn) and biomass production (22%). The interactive impacts of warming and rainfall reduction (W + RR treatment) on plant performance were generally smaller than expected from additive single‐factor effects. 4. Synthesis. Large decreases in plant nutrient pool size and productivity combined with increased mortality during hotter droughts will reduce vegetation cover and nutrient retention capacity, thereby disrupting biogeochemical processes and accelerating dryland degradation with impending climate change. Increased macro‐ and micronutrient co‐limitation of photosynthesis with forecasted climate change conditions may offset any gains in WUEi and productivity derived from anthropogenic CO2 elevation, thereby increasing dryland vegetation vulnerability to drought stress in a warmer and drier climate. The generalized reduction in leaf nutrient contents with warming compromises plant nutritional quality for herbivores, with potential cascading negative effects across trophic levels.This study was supported by the Spanish Ministerio de Economía y Competitividad (projects CGL2010‐21064, CGL2013‐48753‐R and CGL2013‐44661‐R co‐funded by European Union FEDER funds), Fundación Séneca (19477/PI/14) and the European Research Council (ERC Grant agreements 242658 [BIOCOM] and 647038 [BIODESERT]). L.L.‐S. and I.P. acknowledge support from the JAE‐CSIC and Juan de la Cierva Programs (FPDI‐2013‐16221) respectively

Efflux of hydraulically lifted water from mycorrhizal fungal hyphae during imposed drought

Apart from improving plant and soil water status during drought, it has been suggested that hydraulic lift (HL) could enhance plant nutrient capture through the flow of mineral nutrients directly from the soil to plant roots, or by maintaining the functioning of mycorrhizal fungi. We evaluated the extent to which the diel cycle of water availability created by HL covaries with the efflux of HL water from the tips of extramatrical (external) mycorrhizal hyphae, and the possible effects on biogeochemical processes. Phenotypic mycorrhizal fungal variables, such as total and live hyphal lengths, were positively correlated with HL efflux from hyphae, soil water potential (dawn), and plant response variables (foliar 15N). The efflux of HL water from hyphae was also correlated with bacterial abundance and soil enzyme activity (P), and the moistening of soil organic matter. Such findings indicate that the efflux of HL water from the external mycorrhizal mycelia may be a complementary explanation for plant nutrient acquisition and survival during drought