Jordi Martínez-Vilalta

Global convergence in the vulnerability of forests to drought.

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.

Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula

Abstract The summers of 1994 and, to a lesser extent, 1998 were particularly dry in eastern Spain. As a result, several plant species were severely affected. We estimated drought-induced mortality in several populations of three pine species that co-exist in the study area (Pinus nigra, P. pinaster and P. sylvestris). Hydraulic conductivity, vulnerability to xylem embolism, and tree-ring width were also measured for each population. Results showed that mortality only affected P. sylvestris, and that there were significant differences between two populations of this species. Although maximum hydraulic conductivity and vulnerability to embolism were almost identical among species and populations, they differed in other aspects of their hydraulic architecture. In particular, (1) hydraulic conductivity per unit of leaf area was lower in the most acutely affected P. sylvestris population. Lower leaf specific conductivity causes higher water potential gradients and, hence, higher levels of embolism (if vulnerabilities are alike). We suggest that this difference was the main cause of the observed mortality pattern. (2) P. pinaster showed higher water-use efficiency (WUE) (inferred from δ13C data) than the other two species. Regarding the response to drought at the population level, the most affected P. sylvestris population slightly increased growth after the 1994 drought, which we relate to a relaxation of competition among surviving individuals. The important drought-induced mortality observed in the study area suggests that drier climate (as predicted by climate change simulations) may endanger several P. sylvestris populations in the Mediterranean basin.

Size-mediated ageing reduces vigour in trees.

There is increasing interest in understanding the costs and benefits of increased size and prolonged lifespan for plants. Some species of trees can grow more than 100 m in height and can live for several millennia, however whether these achievements are obtained at the cost of some other physiological functions is currently unclear. As increases in size are usually associated with ageing, it is also unclear whether observed reductions in growth rates and increased mortality rates are a function of size or of age per se. One theory proposes that reduced growth after the start of the reproductive phase is caused by cellular senescence. A second set of theories has focussed instead on plant size and the increased respiratory burdens or excessive height. We report on experimental manipulations to separate the effects of extrinsic factors such as size from those of intrinsic factors such as age for four tree species of contrasting phylogeny and life history. For each species, we measured growth, gas exchange and leaf biochemical properties for trees of different ages and sizes in the field and on propagated material obtained from the same genetic individuals but now all of small similar size in our common gardens. For all species, evidence indicated that size, not cellular senescence, accounted for the observed age-related declines in relative growth rates and net assimilation rates. Two species exhibited evidence of genetic control on leaf characters such as specific leaf area, although size also exerted an independent, and stronger, effect. We found partial support for the theory of hydraulic limitations to tree growth. The lack of a marked separation of soma and germline, an unlimited proliferation potential of meristem cells and the exponential increase in reproductive effort with size all help explain the lack of a senescence-induced decline in trees. It is possible that trees much older than the ones we sampled exhibit senescence symptoms.

Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode

• Severe drought may increase physiological stress on long-lived woody vegetation, occasionally leading to mortality of overstory trees. Little is known about the factors determining tree survival and subsequent recovery after drought. • We used structural equation modeling to analyse the recovery of Scots pine (Pinus sylvestris) trees 4 yr after an extreme drought episode occurred in 2004-2005 in north-east Spain. Measured variables included the amount of green foliage, carbon reserves in the stem, mistletoe (Viscum album) infection, needle physiological performance and stem radial growth before, during and after the drought event. • The amount of green leaves and the levels of carbon reserves were related to the impact of drought on radial growth, and mutually correlated. However, our most likely path model indicated that current depletion of carbon reserves was a result of reduced photosynthetic tissue. This relationship potentially constitutes a feedback limiting tree recovery. In addition, mistletoe infection reduced leaf nitrogen content, negatively affecting growth. Finally, successive surveys in 2009-2010 showed a direct association between carbon reserves depletion and drought-induced mortality. • Severe drought events may induce long-term physiological disorders associated with canopy defoliation and depletion of carbon reserves, leading to prolonged recovery of surviving individuals and, eventually, to delayed tree death.

Hydraulic adjustment of Scots pine across Europe.

* The variability of branch-level hydraulic properties was assessed across 12 Scots pine populations covering a wide range of environmental conditions, including some of the southernmost populations of the species. The aims were to relate this variability to differences in climate, and to study the potential tradeoffs between traits. * Traits measured included wood density, radial growth, xylem anatomy, sapwood- and leaf-specific hydraulic conductivity (K(S) and K(L)), vulnerability to embolism, leaf-to-sapwood area ratio (A(L) : A(S)), needle carbon isotope discrimination (Delta13C) and nitrogen content, and specific leaf area. * Between-population variability was high for most of the hydraulic traits studied, but it was directly associated with climate dryness (defined as a combination of atmospheric moisture demand and availability) only for A(L) : A(S), K(L) and Delta13C. Shoot radial growth and A(L) : A(S) declined with stand development, which is consistent with a strategy to avoid exceedingly low water potentials as tree size increases. In addition, we did not find evidence at the intraspecific level of some associations between hydraulic traits that have been commonly reported across species. * The adjustment of Scots pines hydraulic system to local climatic conditions occurred primarily through modifications of A(L) : A(S) and direct stomatal control, whereas intraspecific variation in vulnerability to embolism and leaf physiology appears to be limited.

Drought-Induced Multifactor Decline of Scots Pine in the Pyrenees and Potential Vegetation Change by the Expansion of Co-occurring Oak Species

Episodes of drought-induced tree dieback have been recently observed in many forest areas of the world, particularly at the dry edge of species distributions. Under climate change, those effects could signal potential vegetation shifts occurring over large geographical areas, with major impacts on ecosystem form and function. In this article, we studied the effect of a single drought episode, occurred which in summer 2005, on a Scots pine population in central Pyrenees (NE Spain). Our main objective was to study the environmental correlates of forest decline and vegetation change at the plot level. General and generalized linear models were used to study the relationship between canopy defoliation, mortality and recruitment, and plot characteristics. A drought-driven multifactor dieback was observed in the study forest. Defoliation and mortality were associated with the local level of drought stress estimated at each plot. In addition, stand structure, soil properties, and mistletoe infection were also associated with the observed pattern of defoliation, presumably acting as long-term predisposing factors. Recruitment of Scots pine was low in all plots. In contrast, we observed abundant recruitment of other tree species, mostly Quercus ilex and Q. humilis, particularly in plots where Scots pine showed high defoliation and mortality. These results suggest that an altitudinal upwards migration of Quercus species, mediated by the dieback of the currently dominant species, may take place in the studied slopes. Many rear-edge populations of Scots pine sheltered in the mountain environments of the Iberian Peninsula could be at risk under future climate scenarios.

The hydraulic architecture of Pinaceae – a review

We reviewed the literature to examine the vulnerability to water stress-induced embolism of Pinaceae relative to other conifers and to study the inter-relationships among the main traits involved in the hydraulic function within the Pinaceae. Results showed that Pinaceae (particularly the genus Pinus) are more vulnerable to xylem embolism, and show less variability in this character, than other conifers. Detailed data from 12 populations of Pinaceae (11 species) from three different areas (Piñol and Sala 2000; Martínez-Vilalta and Piñol 2002; Oliveras et al. 2003) was used to study the relationships among hydraulic properties of stems. These included: leaf-to-wood area ratio (AL:AW), wood- and leaf-specific hydraulic conductivity (KW and KL, respectively), vulnerability to xylem embolism (Ψ50PLC), carbon isotope composition of needles (δ13C) and minimum needle water potential (minimum ΨL). Results showed that hydraulic properties tended to be more correlated among each other than with indicators of environmental (precipitation to potential evapotranspiration ratio, P/E) or physiological water stress (minimum ΨL). The only exception was an increase of δ13C with decreasing minimum ΨL and P/E. Overall, AL:AW ratio decreased with increasing vulnerability to xylem embolism, and with increasing KW and KL (P<0.05). We found a strong positive relationship between carbon isotope composition and the estimated maximum loss of conductivity due to xylem embolism under field conditions, suggesting stronger stomatal control in more vulnerable species with higher levels of native embolism. Overall, results are consistent with a range of drought-avoidance strategies to minimise the gradient of water potential through the xylem, and show that different relationships among traits are possible depending on the scale of study (individual vs. species or populations). The strong interdependence among hydraulic traits implies that no single trait is a sufficient predictor of drought-resistance in Pinaceae. Finally, it is hypothesised that the intrinsically vulnerable xylem of pines may limit their survival under extremely dry conditions.

A new look at water transport regulation in plants

Plant function requires effective mechanisms to regulate water transport at a variety of scales. Here, we develop a new theoretical framework describing plant responses to drying soil, based on the relationship between midday and predawn leaf water potentials. The intercept of the relationship (Λ) characterizes the maximum transpiration rate per unit of hydraulic transport capacity, whereas the slope (σ) measures the relative sensitivity of the transpiration rate and plant hydraulic conductance to declining water availability. This framework was applied to a newly compiled global database of leaf water potentials to estimate the values of Λ and σ for 102 plant species. Our results show that our characterization of drought responses is largely consistent within species, and that the parameters Λ and σ show meaningful associations with climate across species. Parameter σ was ≤1 in most species, indicating a tight coordination between the gas and liquid phases of water transport, in which canopy transpiration tended to decline faster than hydraulic conductance during drought, thus reducing the pressure drop through the plant. The quantitative framework presented here offers a new way of characterizing water transport regulation in plants that can be used to assess their vulnerability to drought under current and future climatic conditions.

A hydraulic model to predict drought-induced mortality in woody plants: an application to climate change in the Mediterranean

The potential effects of climate change on vegetation are of increasing concern. In the Mediterranean region, the dominant impact of climate change is expected to be through the modification of water balance. In this paper we present a model developed to predict drought-induced mortality of woody plants under different climatic scenarios. The model is physiologically-based and simulates water transport within individual woody plants, which can be isolated or competing for a common water resource. The model assumes that plant mortality is controlled by the carbon balance: when the plant is unable to transport water to the leaves it ceases to acquire carbon and, if this situation lasts long enough, it can no longer survive. In the particular application that we report in this study, two evergreen species are compared, Quercus ilex and Phillyrea latifolia, which were very differently affected by the acute drought that occurred in E Spain in summer 1994. While in some Q. ilex populations the amount of individuals that dried completely was up to 80%, P. latifolia showed almost no damage. During the years 1999 and 2000, canopy transpiration was monitored using sap-flow sensors in individuals of these two species in a Holm-oak forest from NE Spain. A Generalised Likelihood Uncertainty Estimation (GLUE) approach was used to calibrate the model against sap-flow measurements. The only difference between species that was introduced ‘a priori’ was that Q. ilex was more vulnerable to xylem embolism than P. latifolia (based on our own measurements in the study area). During the calibration process the information provided by the measured sap flows was used to retain the more likely parameter sets for each species. These parameter sets were used in all the following simulations. The model was able to accurately simulate transpiration dynamics of the two species in the study area. When the meteorological conditions of summer 1994 were introduced, the model outputs also reproduced the differential impact that drought had on the two species studied. In the simulations under climate change two factors were explored: the increase in mean temperature (+1.5, +3 and +4.5 °C) through its effect on ET, and the duration of summer drought. Under any of the scenarios, mortalities were much higher for Q. ilex: while this species was predicted to survive with less than 5% mortality droughts of up to 84–94 days, the mortality of P. latifolia reached 5% between days 133 and 150. For droughts longer than 3 months, which is approximately the current drought duration in the study area for dry years, the mortality of Q. ilex increased sharply. These results are discussed in relation to the possible long-term impacts of climate change on Q. ilex-dominated forests.

Structural and climatic determinants of demographic rates of Scots pine forests across the Iberian Peninsula

The demographic rates of tree species typically show large spatial variation across their range. Understanding the environmental factors underlying this variation is a key topic in forest ecology, with far-reaching management implications. Scots pine (Pinus sylvestris L.) covers large areas of the Northern Hemisphere, the Iberian Peninsula being its southwestern distribution limit. In recent decades, an increase in severe droughts and a densification of forests as a result of changes in forest uses have occurred in this region. Our aim was to use climate and stand structure data to explain mortality and growth patterns of Scots pine forests across the Iberian Peninsula. We used data from 2392 plots dominated by Scots pine, sampled for the National Forest Inventory of Spain. Plots were sampled from 1986 to 1996 (IFN2) and were resampled from 1997 to 2007 (IFN3), allowing for the calculation of growth and mortality rates. We fitted linear models to assess the response of growth and mortality rates to the spatial variability of climate, climatic anomalies, and forest structure. Over the period of approximately 10 years between the IFN2 and IFN3, the amount of standing dead trees increased 11-fold. Higher mortality rates were related to dryness, and growth was reduced with increasing dryness and temperature, but results also suggested that effects of climatic stressors were not restricted to dry sites only. Forest structure was strongly related to demographic rates, suggesting that stand development and competition are the main factors associated with demography. In the case of mortality, forest structure interacted with climate, suggesting that competition for water resources induces tree mortality in dry sites. A slight negative relationship was found between mortality and growth, indicating that both rates are likely to be affected by the same stress factors. Additionally, regeneration tended to be lower in plots with higher mortality. Taken together, our results suggest a large-scale self-thinning related to the recent densification of Scots pine forests. This process appears to be enhanced by dry conditions and may lead to a mismatch in forest turnover. Forest management may be an essential adaptive tool under the drier conditions predicted by most climate models.