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.

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.

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.

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.

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.

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.

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.

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.

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.

Fast-slow continuum and reproductive strategies structure plant life-history variation worldwide.

The identification of patterns in life-history strategies across the tree of life is essential to our prediction of population persistence, extinction, and diversification. Plants exhibit a wide range of patterns of longevity, growth, and reproduction, but the general determinants of this enormous variation in life history are poorly understood. We use demographic data from 418 plant species in the wild, from annual herbs to supercentennial trees, to examine how growth form, habitat, and phylogenetic relationships structure plant life histories and to develop a framework to predict population performance. We show that 55% of the variation in plant life-history strategies is adequately characterized using two independent axes: the fast-slow continuum, including fast-growing, short-lived plant species at one end and slow-growing, long-lived species at the other, and a reproductive strategy axis, with highly reproductive, iteroparous species at one extreme and poorly reproductive, semelparous plants with frequent shrinkage at the other. Our findings remain consistent across major habitats and are minimally affected by plant growth form and phylogenetic ancestry, suggesting that the relative independence of the fast-slow and reproduction strategy axes is general in the plant kingdom. Our findings have similarities with how life-history strategies are structured in mammals, birds, and reptiles. The position of plant species populations in the 2D space produced by both axes predicts their rate of recovery from disturbances and population growth rate. This life-history framework may complement trait-based frameworks on leaf and wood economics; together these frameworks may allow prediction of responses of plants to anthropogenic disturbances and changing environments.

Trends in tropical tree growth: re-analyses confirm earlier findings.

In a recent Opinion article, Brienen et al. (2016) raise doubts about our finding that tropical tree growth has not increased during 150 years of CO2 rise (Groenendijk et al., 2015; van der Sleen et al., 2015). They claim that our tree-ring data contain evidence for historical growth stimulation that was concealed due to failing regeneration in several species. Here we show that (i) the correction method proposed by Brienen et al. induces a bias towards finding positive growth trends, (ii) the results of Brienen et al. rest on selective removal of species, (iii) there is a simple and effective way to accommodate effects of recruitment failure by subsetting data, and (iv) the application of this method confirms our earlier findings. Thus, our results are robust to effects of recruitment failure and our conclusions remain unchanged: we find no evidence for historical growth changes in our studied tree species.

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.

Loss of animal seed dispersal increases extinction risk in a tropical tree species due to pervasive negative density dependence across life stages.

Overhunting in tropical forests reduces populations of vertebrate seed dispersers. If reduced seed dispersal has a negative impact on tree population viability, overhunting could lead to altered forest structure and dynamics, including decreased biodiversity. However, empirical data showing decreased animal-dispersed tree abundance in overhunted forests contradict demographic models which predict minimal sensitivity of tree population growth rate to early life stages. One resolution to this discrepancy is that seed dispersal determines spatial aggregation, which could have demographic consequences for all life stages. We tested the impact of dispersal loss on population viability of a tropical tree species, Miliusa horsfieldii, currently dispersed by an intact community of large mammals in a Thai forest. We evaluated the effect of spatial aggregation for all tree life stages, from seeds to adult trees, and constructed simulation models to compare population viability with and without animal-mediated seed dispersal. In simulated populations, disperser loss increased spatial aggregation by fourfold, leading to increased negative density dependence across the life cycle and a 10-fold increase in the probability of extinction. Given that the majority of tree species in tropical forests are animal-dispersed, overhunting will potentially result in forests that are fundamentally different from those existing now.

Tree growth variation in the tropical forest: understanding effects of temperature, rainfall and CO2.

Tropical forest responses to climatic variability have important consequences for global carbon cycling, but are poorly understood. As empirical, correlative studies cannot disentangle the interactive effects of climatic variables on tree growth, we used a tree growth model (IBTREE) to unravel the climate effects on different physiological pathways and in turn on stem growth variation. We parameterized the model for canopy trees of Toona ciliata (Meliaceae) from a Thai monsoon forest and compared predicted and measured variation from a tree-ring study over a 30-year period. We used historical climatic variation of minimum and maximum day temperature, precipitation and carbon dioxide (CO2 ) in different combinations to estimate the contribution of each climate factor in explaining the inter-annual variation in stem growth. Running the model with only variation in maximum temperature and rainfall yielded stem growth patterns that explained almost 70% of the observed inter-annual variation in stem growth. Our results show that maximum temperature had a strong negative effect on the stem growth by increasing respiration, reducing stomatal conductance and thus mitigating a higher transpiration demand, and - to a lesser extent - by directly reducing photosynthesis. Although stem growth was rather weakly sensitive to rain, stem growth variation responded strongly and positively to rainfall variation owing to the strong inter-annual fluctuations in rainfall. Minimum temperature and atmospheric CO2 concentration did not significantly contribute to explaining the inter-annual variation in stem growth. Our innovative approach - combining a simulation model with historical data on tree-ring growth and climate - allowed disentangling the effects of strongly correlated climate variables on growth through different physiological pathways. Similar studies on different species and in different forest types are needed to further improve our understanding of the sensitivity of tropical tree growth to climatic variability and change.