Constraining long-term model predictions for woody growth using tropical tree rings.

The strength and persistence of the tropical carbon sink hinges on the long-term responses of woody growth to climatic variations and increasing CO2 . However, the sensitivity of tropical woody growth to these environmental changes is poorly understood, leading to large uncertainties in growth predictions. Here, we used tree ring records from a Southeast Asian tropical forest to constrain ED2.2-hydro, a terrestrial biosphere model with explicit vegetation demography. Specifically, we assessed individual-level woody growth responses to historical climate variability and increases in atmospheric CO2 (Ca ). When forced with historical Ca , ED2.2-hydro reproduced the magnitude of increases in intercellular CO2 concentration (a major determinant of photosynthesis) estimated from tree ring carbon isotope records. In contrast, simulated growth trends were considerably larger than those obtained from tree rings, suggesting that woody biomass production efficiency (WBPE = woody biomass production:gross primary productivity) was overestimated by the model. The estimated WBPE decline under increasing Ca based on model-data discrepancy was comparable to or stronger than (depending on tree species and size) the observed WBPE changes from a multi-year mature-forest CO2 fertilization experiment. In addition, we found that ED2.2-hydro generally overestimated climatic sensitivity of woody growth, especially for late-successional plant functional types. The model-data discrepancy in growth sensitivity to climate was likely caused by underestimating WBPE in hot and dry years due to commonly used model assumptions on carbon use efficiency and allocation. To our knowledge, this is the first study to constrain model predictions of individual tree-level growth sensitivity to Ca and climate against tropical tree-ring data. Our results suggest that improving model processes related to WBPE is crucial to obtain better predictions of tropical forest responses to droughts and increasing Ca . More accurate parameterization of WBPE will likely reduce the stimulation of woody growth by Ca rise predicted by biosphere models.

Diel and seasonal stem growth responses to climatic variation are consistent across species in a subtropical tree community.

Understanding how intra-annual stem growth responds to atmospheric and soil conditions is essential for assessing the effects of climate extremes on forest productivity. In species-poor forests, such understanding can be obtained by studying stem growth of the dominant species. Yet, in species-rich (sub-)tropical forests, it is unclear whether these responses are consistent among species. We monitored intra-annual stem growth with high-resolution dendrometers for 27 trees belonging to 14 species over 5 yr in a montane subtropical forest. We quantified diel and seasonal stem growth patterns, verified to what extent observed growth patterns coincide across species and analysed their main climatic drivers. We found very consistent intra-annual growth patterns across species. Species varied in the rate but little in the timing of growth. Diel growth patterns revealed that - across species - trees mainly grew before dawn when vapour pressure deficit (VPD) was low. Within the year, trees mainly grew between May and August driven by temperature and VPD, but not by soil moisture. Our study reveals highly consistent stem growth patterns and climatic drivers at community level. Further studies are needed to verify whether these results hold across climates and forests, and whether they can be scaled up to estimate forest productivity.

High vapour pressure deficit enhances turgor limitation of stem growth in an Asian tropical rainforest tree.

Tropical forests are experiencing increases in vapour pressure deficit (D), with possible negative impacts on tree growth. Tree-growth reduction due to rising D is commonly attributed to carbon limitation, thus overlooking the potentially important mechanism of D-induced impairment of wood formation due to an increase in turgor limitation. Here we calibrate a mechanistic tree-growth model to simulate turgor limitation of radial stem growth in mature Toona cilitata trees in an Asian tropical forest. Hourly sap flow and dendrometer measurements were collected to simulate turgor-driven growth during the growing season. Simulated seasonal patterns of radial stem growth matched well with growth observations. Growth mainly occurred at night and its pre-dawn build-up appeared to be limited under higher D. Across seasons, the night-time turgor pressure required for growth was negatively related to previous midday D, possibly due to a relatively high canopy conductance at high D, relative to stem rehydration. These findings provide the first evidence that tropical trees grow at night and that turgor pressure limits tree growth. We suggest including turgor limitation of tree stem growth in models also for tropical forest carbon dynamics, in particular, if these models simulate effects of warming and increased frequency of droughts.

Restoration success in former Amazonian mines is driven by soil amendment and forest proximity.

Mining contributes importantly to tropical deforestation and land degradation. To mitigate these effects, mining companies are increasingly obliged to restore abandoned mine lands, but factors driving restoration success are hardly evaluated. Here, we investigate the influence of ecological factors (restoration age, soil properties and surrounding forest area) and management factors (diversity and density of planted species, mine zone) on the recovery rate of forest structure and tree diversity on 40 post-mining restoration areas in Southern Amazonia, Brazil, using a 9-year annual monitoring dataset consisting of over 25 000 trees. We found that recovery of forest structure was closely associated with interactions between soil quality and the planted tree communities, and that tree diversity recovery was positively associated with the amount of surrounding forests. We also observed that forest structure and diversity recover more slowly in mine tailings compared to pit surroundings. Our study confirms the complexity of mine land restoration but also reveals that planting design and soil improvement can increase restoration success. For resource-efficient mine restoration, we recommend the focusing of efforts on tailings, which are hardest to restore, and reducing efforts in pit surroundings and areas close to surrounding forest because of their potential for restoration by natural regeneration. This article is part of the theme issue 'Understanding forest landscape restoration: reinforcing scientific foundations for the UN Decade on Ecosystem Restoration'.

Clay and soil organic matter drive wood multi-elemental composition of a tropical tree species: Implications for timber tracing.

Forensic methods to independently trace timber origin are essential to combat illegal timber trade. Tracing product origin by analysing their multi-element composition has been successfully applied in several commodities, but its potential for timber is not yet known. To evaluate this potential the drivers of wood multi-elemental composition need to be studied. Here we report on the first study relating wood multi-elemental composition of forest trees to soil chemical and physical properties. We studied the reactive soil element pools and the multi-elemental composition in sapwood and heartwood for 37 Azobé (Lophira alata) trees at two forest sites in Cameroon. A total of 46 elements were measured using ICP-MS. We also measured three potential drivers of soil and wood elemental composition: clay content, soil organic matter and pH. We tested associations between soil and wood using multiple regressions and multivariate analyses (Mantel test, db-RDA). Finally, we performed a Random Forest analysis of heartwood elemental composition to check site assignment accuracy. We found elemental compositions of soil, sapwood and heartwood to be significantly associated. Soil clay content and organic matter positively influenced individual element concentrations (for 13 and 9 elements out of 46 respectively) as well as the multi-elemental composition in wood. However, associations between wood and topsoil elemental concentrations were only significant for one element. We found close associations between element concentrations and composition in sapwood and heartwood. Lastly, the Random Forest assignment success was 97.3 %. Our findings indicate that wood elemental composition is associated with that in the topsoil and its variation is related to soil clay and organic matter content. These associations suggests that the multi-elemental composition of wood can yield chemical fingerprints obtained from sites that differ in soil properties. This finding in addition to the high assignment accuracy shows potential of multi-element analysis for tracing wood origin.

The role of demographic compensation in stabilising marginal tree populations in North America.

Demographic compensation-the opposing responses of vital rates along environmental gradients-potentially delays anticipated species' range contraction under climate change, but no consensus exists on its actual contribution. We calculated population growth rate (λ) and demographic compensation across the distributional ranges of 81 North American tree species and examined their responses to simulated warming and tree competition. We found that 43% of species showed stable population size at both northern and southern edges. Demographic compensation was detected in 25 species, yet 15 of them still showed a potential retraction from southern edges, indicating that compensation alone cannot maintain range stability. Simulated climatic warming caused larger decreases in λ for most species and weakened the effectiveness of demographic compensation in stabilising ranges. These findings suggest that climate stress may surpass the limited capacity of demographic compensation and pose a threat to the viability of North American tree populations.

Species-level tree crown maps improve predictions of tree recruit abundance in a tropical landscape.

Predicting forest recovery at landscape scales will aid forest restoration efforts. The first step in successful forest recovery is tree recruitment. Forecasts of tree recruit abundance, derived from the landscape-scale distribution of seed sources (i.e., adult trees), could assist efforts to identify sites with high potential for natural regeneration. However, previous work revealed wide variation in the effect of seed sources on seedling abundance, from positive to no effect. We quantified the relationship between adult tree seed sources and tree recruits and predicted where natural recruitment would occur in a fragmented, tropical, agricultural landscape. We integrated species-specific tree crown maps generated from hyperspectral imagery and property ownership data with field data on the spatial distribution of tree recruits from five species. We then developed hierarchical Bayesian models to predict landscape-scale recruit abundance. Our models revealed that species-specific maps of tree crowns improved recruit abundance predictions. Conspecific crown area had a much stronger impact on recruitment abundance (8.00% increase in recruit abundance when conspecific tree density increases from zero to one tree; 95% credible interval (CI): 0.80% to 11.57%) than heterospecific crown area (0.03% increase with the addition of a single heterospecific tree, 95% CI: -0.60% to 0.68%). Individual property ownership was also an important predictor of recruit abundance: The best performing model had varying effects of conspecific and heterospecific crown area on recruit abundance, depending on individual property ownership. We demonstrate how novel remote sensing approaches and cadastral data can be used to generate high-resolution and landscape-level maps of tree recruit abundance. Spatial models parameterized with field, cadastral, and remote sensing data are poised to assist decision support for forest landscape restoration.

Interannual temperature variability is a principal driver of low-frequency fluctuations in marine fish populations.

Marine fish populations commonly exhibit low-frequency fluctuations in biomass that can cause catch volatility and thus endanger the food and economic security of dependent coastal societies. Such variability has been linked to fishing intensity, demographic processes and environmental variability, but our understanding of the underlying drivers remains poor for most fish stocks. Our study departs from previous findings showing that sea surface temperature (SST) is a significant driver of fish somatic growth variability and that life-history characteristics mediate population-level responses to environmental variability. We use autoregressive models to simulate how fish populations integrate SST variability over multiple years depending on fish life span and trophic position. We find that simulated SST-driven population dynamics can explain a significant portion of observed low-frequency variability in independent observations of fisheries landings around the globe. Predictive skill, however, decreases with increasing fishing pressure, likely due to demographic truncation. Using our modelling approach, we also show that increases in the mean and variance of SST could amplify biomass volatility and lessen its predictability in the future. Overall, biological integration of high-frequency SST variability represents a null hypothesis with which to explore the drivers of low-frequency population change across upper-trophic marine species.

Joint effects of climate, tree size, and year on annual tree growth derived from tree-ring records of ten globally distributed forests.

Tree rings provide an invaluable long-term record for understanding how climate and other drivers shape tree growth and forest productivity. However, conventional tree-ring analysis methods were not designed to simultaneously test effects of climate, tree size, and other drivers on individual growth. This has limited the potential to test ecologically relevant hypotheses on tree growth sensitivity to environmental drivers and their interactions with tree size. Here, we develop and apply a new method to simultaneously model nonlinear effects of primary climate drivers, reconstructed tree diameter at breast height (DBH), and calendar year in generalized least squares models that account for the temporal autocorrelation inherent to each individual tree's growth. We analyze data from 3811 trees representing 40 species at 10 globally distributed sites, showing that precipitation, temperature, DBH, and calendar year have additively, and often interactively, influenced annual growth over the past 120 years. Growth responses were predominantly positive to precipitation (usually over ≥3-month seasonal windows) and negative to temperature (usually maximum temperature, over ≤3-month seasonal windows), with concave-down responses in 63% of relationships. Climate sensitivity commonly varied with DBH (45% of cases tested), with larger trees usually more sensitive. Trends in ring width at small DBH were linked to the light environment under which trees established, but basal area or biomass increments consistently reached maxima at intermediate DBH. Accounting for climate and DBH, growth rate declined over time for 92% of species in secondary or disturbed stands, whereas growth trends were mixed in older forests. These trends were largely attributable to stand dynamics as cohorts and stands age, which remain challenging to disentangle from global change drivers. By providing a parsimonious approach for characterizing multiple interacting drivers of tree growth, our method reveals a more complete picture of the factors influencing growth than has previously been possible.

Climate-driven, but dynamic and complex? A reconciliation of competing hypotheses for species' distributions.

Estimates of the percentage of species "committed to extinction" by climate change range from 15% to 37%. The question is whether factors other than climate need to be included in models predicting species' range change. We created demographic range models that include climate vs. climate-plus-competition, evaluating their influence on the geographic distribution of Pinus edulis, a pine endemic to the semiarid southwestern U.S. Analyses of data on 23,426 trees in 1941 forest inventory plots support the inclusion of competition in range models. However, climate and competition together only partially explain this species' distribution. Instead, the evidence suggests that climate affects other range-limiting processes, including landscape-scale, spatial processes such as disturbances and antagonistic biotic interactions. Complex effects of climate on species distributions-through indirect effects, interactions, and feedbacks-are likely to cause sudden changes in abundance and distribution that are not predictable from a climate-only perspective.

Detecting forest response to droughts with global observations of vegetation water content.

Droughts in a warming climate have become more common and more extreme, making understanding forest responses to water stress increasingly pressing. Analysis of water stress in trees has long focused on water potential in xylem and leaves, which influences stomatal closure and water flow through the soil-plant-atmosphere continuum. At the same time, changes of vegetation water content (VWC) are linked to a range of tree responses, including fluxes of water and carbon, mortality, flammability, and more. Unlike water potential, which requires demanding in situ measurements, VWC can be retrieved from remote sensing measurements, particularly at microwave frequencies using radar and radiometry. Here, we highlight key frontiers through which VWC has the potential to significantly increase our understanding of forest responses to water stress. To validate remote sensing observations of VWC at landscape scale and to better relate them to data assimilation model parameters, we introduce an ecosystem-scale analog of the pressure-volume curve, the non-linear relationship between average leaf or branch water potential and water content commonly used in plant hydraulics. The sources of variability in these ecosystem-scale pressure-volume curves and their relationship to forest response to water stress are discussed. We further show to what extent diel, seasonal, and decadal dynamics of VWC reflect variations in different processes relating the tree response to water stress. VWC can also be used for inferring belowground conditions-which are difficult to impossible to observe directly. Lastly, we discuss how a dedicated geostationary spaceborne observational system for VWC, when combined with existing datasets, can capture diel and seasonal water dynamics to advance the science and applications of global forest vulnerability to future droughts.

Recent CO2 rise has modified the sensitivity of tropical tree growth to rainfall and temperature.

Atmospheric CO2 (ca ) rise changes the physiology and possibly growth of tropical trees, but these effects are likely modified by climate. Such ca  × climate interactions importantly drive CO2 fertilization effects of tropical forests predicted by global vegetation models, but have not been tested empirically. Here we use tree-ring analyses to quantify how ca rise has shifted the sensitivity of tree stem growth to annual fluctuations in rainfall and temperature. We hypothesized that ca rise reduces drought sensitivity and increases temperature sensitivity of growth, by reducing transpiration and increasing leaf temperature. These responses were expected for cooler sites. At warmer sites, ca rise may cause leaf temperatures to frequently exceed the optimum for photosynthesis, and thus induce increased drought sensitivity and stronger negative effects of temperature. We tested these hypotheses using measurements of 5,318 annual rings from 129 trees of the widely distributed (sub-)tropical tree species, Toona ciliata. We studied growth responses during 1950-2014, a period during which ca rose by 28%. Tree-ring data were obtained from two cooler (mean annual temperature: 20.5-20.7°C) and two warmer (23.5-24.8°C) sites. We tested ca  × climate interactions, using mixed-effect models of ring-width measurements. Our statistical models revealed several significant and robust ca  × climate interactions. At cooler sites (and seasons), ca  × climate interactions showed good agreement with hypothesized growth responses of reduced drought sensitivity and increased temperature sensitivity. At warmer sites, drought sensitivity increased with increasing ca , as predicted, and hot years caused stronger growth reduction at high ca . Overall, ca rise has significantly modified sensitivity of Toona stem growth to climatic variation, but these changes depended on mean climate. Our study suggests that effects of ca rise on tropical tree growth may be more complex and less stimulatory than commonly assumed and require a better representation in global vegetation models.

Long-term physiological and growth responses of Himalayan fir to environmental change are mediated by mean climate.

High-elevation forests are experiencing high rates of warming, in combination with CO2 rise and (sometimes) drying trends. In these montane systems, the effects of environmental changes on tree growth are also modified by elevation itself, thus complicating our ability to predict effects of future climate change. Tree-ring analysis along an elevation gradient allows quantifying effects of gradual and annual environmental changes. Here, we study long-term physiological (ratio of internal to ambient CO2 , i.e., Ci /Ca and intrinsic water-use efficiency, iWUE) and growth responses (tree-ring width) of Himalayan fir (Abies spectabilis) trees in response to warming, drying, and CO2 rise. Our study was conducted along elevational gradients in a dry and a wet region in the central Himalaya. We combined dendrochronology and stable carbon isotopes (δ13 C) to quantify long-term trends in Ci /Ca ratio and iWUE (δ13 C-derived), growth (mixed-effects models), and evaluate climate sensitivity (correlations). We found that iWUE increased over time at all elevations, with stronger increase in the dry region. Climate-growth relations showed growth-limiting effects of spring moisture (dry region) and summer temperature (wet region), and negative effects of temperature (dry region). We found negative growth trends at lower elevations (dry and wet regions), suggesting that continental-scale warming and regional drying reduced tree growth. This interpretation is supported by δ13 C-derived long-term physiological responses, which are consistent with responses to reduced moisture and increased vapor pressure deficit. At high elevations (wet region), we found positive growth trends, suggesting that warming has favored tree growth in regions where temperature most strongly limits growth. At lower elevations (dry and wet regions), the positive effects of CO2 rise did not mitigate the negative effects of warming and drying on tree growth. Our results raise concerns on the productivity of Himalayan fir forests at low and middle (<3,300 m) elevations as climate change progresses.

Heritability of growth and leaf loss compensation in a long-lived tropical understorey palm.

INTRODUCTION: Defoliation and light competition are ubiquitous stressors that can strongly limit plant performance. Tolerance to defoliation is often associated with compensatory growth, which could be positively or negatively related to plant growth. Genetic variation in growth, tolerance and compensation, in turn, plays an important role in the evolutionary adaptation of plants to changing disturbance regimes but this issue has been poorly investigated for long-lived woody species. We quantified genetic variation in plant growth and growth parameters, tolerance to defoliation and compensation for a population of the understorey palm Chamaedorea elegans. In addition, we evaluated genetic correlations between growth and tolerance/compensation. METHODS: We performed a greenhouse experiment with 711 seedlings from 43 families with twelve or more individuals of C. elegans. Seeds were collected in southeast Mexico within a 0.7 ha natural forest area. A two-third defoliation treatment (repeated every two months) was applied to half of the individuals to simulate leaf loss. Compensatory responses in specific leaf area, biomass allocation to leaves and growth per unit leaf area were quantified using iterative growth models. RESULTS: We found that growth rate was highly heritable and that plants compensated strongly for leaf loss. However, genetic variation in tolerance, compensation, and the individual compensatory responses was low. We found strong correlations between family mean growth rates in control and defoliation treatments. We did not find indications for growth-tolerance/compensation trade-offs: genetic correlation between tolerance/compensation and growth rate were not significant. IMPLICATIONS: The high genetic variation in growth rate, but low genetic variation in tolerance and compensation observed here suggest high ability to adapt to changes in environment that require different growth rates, but a low potential for evolutionary adaptation to changes in damage or herbivory. The strong correlations between family mean growth rates in control and defoliation treatments suggest that performance differences among families are also maintained under stress of disturbance.

Compositional response of Amazon forests to climate change.

Most of the planet's diversity is concentrated in the tropics, which includes many regions undergoing rapid climate change. Yet, while climate-induced biodiversity changes are widely documented elsewhere, few studies have addressed this issue for lowland tropical ecosystems. Here we investigate whether the floristic and functional composition of intact lowland Amazonian forests have been changing by evaluating records from 106 long-term inventory plots spanning 30 years. We analyse three traits that have been hypothesized to respond to different environmental drivers (increase in moisture stress and atmospheric CO2 concentrations): maximum tree size, biogeographic water-deficit affiliation and wood density. Tree communities have become increasingly dominated by large-statured taxa, but to date there has been no detectable change in mean wood density or water deficit affiliation at the community level, despite most forest plots having experienced an intensification of the dry season. However, among newly recruited trees, dry-affiliated genera have become more abundant, while the mortality of wet-affiliated genera has increased in those plots where the dry season has intensified most. Thus, a slow shift to a more dry-affiliated Amazonia is underway, with changes in compositional dynamics (recruits and mortality) consistent with climate-change drivers, but yet to significantly impact whole-community composition. The Amazon observational record suggests that the increase in atmospheric CO2 is driving a shift within tree communities to large-statured species and that climate changes to date will impact forest composition, but long generation times of tropical trees mean that biodiversity change is lagging behind climate change.

A Wood Biology Agenda to Support Global Vegetation Modelling.

Realistic forecasting of forest responses to climate change critically depends on key advancements in global vegetation modelling. Compared with traditional 'big-leaf' models that simulate forest stands, 'next-generation' vegetation models aim to track carbon-, light-, water-, and nutrient-limited growth of individual trees. Wood biology can play an important role in delivering the required knowledge at tissue-to-individual levels, at minute-to-century scales and for model parameterization and benchmarking. We propose a wood biology research agenda that contributes to filling six knowledge gaps: sink versus source limitation, drivers of intra-annual growth, drought impacts, functional wood traits, dynamic biomass allocation, and nutrient cycling. Executing this agenda will expedite model development and increase the ability of models to forecast global change impact on forest dynamics.

Explaining long-term inter-individual growth variation in plant populations: persistence of abiotic factors matters.

An unanswered question in ecology is whether the environmental factors driving short-term performance also determine the often observed long-term performance differences among individuals. Here, we analyze the extent to which temporal persistence of spatial heterogeneity in environmental factors can contribute to long-term inter-individual variation in stem length growth. For a natural population of a long-lived understorey palm, we first quantified the effect of several environmental factors on stem length growth and survival. We then performed individual-based simulations of growth trajectories, in which we varied, for two environmental factors: (1) the strength of the effect on stem length growth and (2) the temporal persistence. Short-term variation in stem length growth was strongly driven by light availability. Auto-correlation in light availability and soil pH increased simulated variation in stem length growth among 20-year-old palms to levels similar to the observed variation. Analyses in which we varied both the strength of the effect on stem length growth and the temporal persistence of the environmental factors revealed that a large fraction of observed long-term growth differences can be explained, as long as one of these effects is strong. This implies that environmental factors that are relatively unimportant for short-term performance can still drive long-term performance differences when the environmental variation is sufficiently persistent over time.