Maurizio Mencuccini

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 Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely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.

The human footprint in the carbon cycle of temperate and boreal forests

Temperate and boreal forests in the Northern Hemisphere cover an area of about 2 × 107 square kilometres and act as a substantial carbon sink (0.6–0.7 petagrams of carbon per year). Although forest expansion following agricultural abandonment is certainly responsible for an important fraction of this carbon sink activity, the additional effects on the carbon balance of established forests of increased atmospheric carbon dioxide, increasing temperatures, changes in management practices and nitrogen deposition are difficult to disentangle, despite an extensive network of measurement stations. The relevance of this measurement effort has also been questioned, because spot measurements fail to take into account the role of disturbances, either natural (fire, pests, windstorms) or anthropogenic (forest harvesting). Here we show that the temporal dynamics following stand-replacing disturbances do indeed account for a very large fraction of the overall variability in forest carbon sequestration. After the confounding effects of disturbance have been factored out, however, forest net carbon sequestration is found to be overwhelmingly driven by nitrogen deposition, largely the result of anthropogenic activities. The effect is always positive over the range of nitrogen deposition covered by currently available data sets, casting doubts on the risk of widespread ecosystem nitrogen saturation under natural conditions. The results demonstrate that mankind is ultimately controlling the carbon balance of temperate and boreal forests, either directly (through forest management) or indirectly (through nitrogen deposition).

Improved allometric models to estimate the aboveground biomass of tropical trees

Terrestrial carbon stock mapping is important for the successful implementation of climate change mitigation policies. Its accuracy depends on the availability of reliable allometric models to infer oven-dry aboveground biomass of trees from census data. The degree of uncertainty associated with previously published pantropical aboveground biomass allometries is large. We analyzed a global database of directly harvested trees at 58 sites, spanning a wide range of climatic conditions and vegetation types (4004 trees ≥ 5 cm trunk diameter). When trunk diameter, total tree height, and wood specific gravity were included in the aboveground biomass model as covariates, a single model was found to hold across tropical vegetation types, with no detectable effect of region or environmental factors. The mean percent bias and variance of this model was only slightly higher than that of locally fitted models. Wood specific gravity was an important predictor of aboveground biomass, especially when including a much broader range of vegetation types than previous studies. The generic tree diameter-height relationship depended linearly on a bioclimatic stress variable E, which compounds indices of temperature variability, precipitation variability, and drought intensity. For cases in which total tree height is unavailable for aboveground biomass estimation, a pantropical model incorporating wood density, trunk diameter, and the variable E outperformed previously published models without height. However, to minimize bias, the development of locally derived diameter-height relationships is advised whenever possible. Both new allometric models should contribute to improve the accuracy of biomass assessment protocols in tropical vegetation types, and to advancing our understanding of architectural and evolutionary constraints on woody plant development.

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.

Death from drought in tropical forests is triggered by hydraulics not carbon starvation

Drought threatens tropical rainforests over seasonal to decadal timescales, but the drivers of tree mortality following drought remain poorly understood. It has been suggested that reduced availability of non-structural carbohydrates (NSC) critically increases mortality risk through insufficient carbon supply to metabolism (‘carbon starvation’). However, little is known about how NSC stores are affected by drought, especially over the long term, and whether they are more important than hydraulic processes in determining drought-induced mortality. Using data from the world’s longest-running experimental drought study in tropical rainforest (in the Brazilian Amazon), we test whether carbon starvation or deterioration of the water-conducting pathways from soil to leaf trigger tree mortality. Biomass loss from mortality in the experimentally droughted forest increased substantially after >10 years of reduced soil moisture availability. The mortality signal was dominated by the death of large trees, which were at a much greater risk of hydraulic deterioration than smaller trees. However, we find no evidence that the droughted trees suffered carbon starvation, as their NSC concentrations were similar to those of non-droughted trees, and growth rates did not decline in either living or dying trees. Our results indicate that hydraulics, rather than carbon starvation, triggers tree death from drought in tropical rainforest.

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.

Linking phloem function to structure: Analysis with a coupled xylem–phloem transport model

We carried out a theoretical analysis of phloem transport based on Münch hypothesis by developing a coupled xylem-phloem transport model. Results showed that the maximum sugar transport rate of the phloem was limited by solution viscosity and that transport requirements were strongly affected by prevailing xylem water potential. The minimum number of xylem and phloem conduits required to sustain transpiration and assimilation, respectively, were calculated. At its maximum sugar transport rate, the phloem functioned with a high turgor pressure difference between the sugar sources and sinks but the turgor pressure difference was reduced if additional parallel conduits were added or solute relays were introduced. Solute relays were shown to decrease the number of parallel sieve tubes needed for phloem transport, leading to a more uniform turgor pressure and allowing faster information transmission within the phloem. Because xylem water potential affected both xylem and phloem transport, the conductance of the two systems was found to be coupled such that large structural investments in the xylem reduced the need for investment in the phloem and vice versa.

Capacitive effect of cavitation in xylem conduits: results from a dynamic model

Embolisms decrease plant hydraulic conductance and therefore reduce the ability of the xylem to transport water to leaves provided that embolized conduits are not refilled. However, as a xylem conduit is filled with gas during cavitation, water is freed to the transpiration stream and this transiently increases xylem water potential. This capacitive effect of embolism formation on plant function has not been explicitly quantified in the past. A dynamic model is presented that models xylem water potential, xylem sap flow and cavitation, taking into account both the decreasing hydraulic conductance and the water release effect of xylem embolism. The significance of the capacitive effect increases in relation to the decreasing hydraulic conductance effect when transpiration rate is low in relation to the total amount of water in xylem conduits. This ratio is typically large in large trees and during drought.

Thirty years of seed production in a subalpine Norway spruce forest: Patterns of temporal and spatial variation

Abstract Norway spruce seed production was studied over 30 years in a subalpine forest of the south-eastern Alps. Thirteen locations were selected along a gradient of elevation and aspect. During mast years, seed production declined on average by about 100 seeds m−2 year−1 per 100 m elevation. The increase in elevation was associated with a reduction in mast year frequency and average mast production. A complex of climatic and edaphic factors appeared to be responsible for the reduction in seed production along the elevation gradient. North-facing locations produced significantly more seeds per square metre per year than south-facing locations. This difference was probably linked with frequent water stresses on south-facing slopes. Variability in seed production within the forest was pronounced and unpredictable in low-production years. The tendency to concentrate seed crops, especially during mast years was not influenced by stand characteristics. The proportion of full seeds and the proportion of seeds which survived vertebrate predation were higher during mast years. These results are interpreted in the context of Norway spruce population dynamics.

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.The mechanisms underlying drought-induced tree mortality are not fully resolved. Here, the authors show that, across multiple tree species, loss of xylem conductivity above 60% is associated with mortality, while carbon starvation is not universal.