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.

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.

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.

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.

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.

Tree Age Distributions Reveal Large-Scale Disturbance-Recovery Cycles in Three Tropical Forests.

Over the past few decades there has been a growing realization that a large share of apparently 'virgin' or 'old-growth' tropical forests carries a legacy of past natural or anthropogenic disturbances that have a substantial effect on present-day forest composition, structure and dynamics. Yet, direct evidence of such disturbances is scarce and comparisons of disturbance dynamics across regions even more so. Here we present a tree-ring based reconstruction of disturbance histories from three tropical forest sites in Bolivia, Cameroon, and Thailand. We studied temporal patterns in tree regeneration of shade-intolerant tree species, because establishment of these trees is indicative for canopy disturbance. In three large areas (140-300 ha), stem disks and increment cores were collected for a total of 1154 trees (>5 cm diameter) from 12 tree species to estimate the age of every tree. Using these age estimates we produced population age distributions, which were analyzed for evidence of past disturbance. Our approach allowed us to reconstruct patterns of tree establishment over a period of around 250 years. In Bolivia, we found continuous regeneration rates of three species and a peaked age distribution of a long-lived pioneer species. In both Cameroon and Thailand we found irregular age distributions, indicating strongly reduced regeneration rates over a period of 10-60 years. Past fires, windthrow events or anthropogenic disturbances all provide plausible explanations for the reported variation in tree age across the three sites. Our results support the recent idea that the long-term dynamics of tropical forests are impacted by large-scale disturbance-recovery cycles, similar to those driving temperate forest dynamics.

(15)N in tree rings as a bio-indicator of changing nitrogen cycling in tropical forests: an evaluation at three sites using two sampling methods.

Anthropogenic nitrogen deposition is currently causing a more than twofold increase of reactive nitrogen input over large areas in the tropics. Elevated (15)N abundance (δ(15)N) in the growth rings of some tropical trees has been hypothesized to reflect an increased leaching of (15)N-depleted nitrate from the soil, following anthropogenic nitrogen deposition over the last decades. To find further evidence for altered nitrogen cycling in tropical forests, we measured long-term δ(15)N values in trees from Bolivia, Cameroon, and Thailand. We used two different sampling methods. In the first, wood samples were taken in a conventional way: from the pith to the bark across the stem of 28 large trees (the "radial" method). In the second, δ(15)N values were compared across a fixed diameter (the "fixed-diameter" method). We sampled 400 trees that differed widely in size, but measured δ(15)N in the stem around the same diameter (20 cm dbh) in all trees. As a result, the growth rings formed around this diameter differed in age and allowed a comparison of δ(15)N values over time with an explicit control for potential size-effects on δ(15)N values. We found a significant increase of tree-ring δ(15)N across the stem radius of large trees from Bolivia and Cameroon, but no change in tree-ring δ(15)N values over time was found in any of the study sites when controlling for tree size. This suggests that radial trends of δ(15)N values within trees reflect tree ontogeny (size development). However, for the trees from Cameroon and Thailand, a low statistical power in the fixed-diameter method prevents to conclude this with high certainty. For the trees from Bolivia, statistical power in the fixed-diameter method was high, showing that the temporal trend in tree-ring δ(15)N values in the radial method is primarily caused by tree ontogeny and unlikely by a change in nitrogen cycling. We therefore stress to account for tree size before tree-ring δ(15)N values can be properly interpreted.

No evidence for consistent long-term growth stimulation of 13 tropical tree species: results from tree-ring analysis.

The important role of tropical forests in the global carbon cycle makes it imperative to assess changes in their carbon dynamics for accurate projections of future climate-vegetation feedbacks. Forest monitoring studies conducted over the past decades have found evidence for both increasing and decreasing growth rates of tropical forest trees. The limited duration of these studies restrained analyses to decadal scales, and it is still unclear whether growth changes occurred over longer time scales, as would be expected if CO2 -fertilization stimulated tree growth. Furthermore, studies have so far dealt with changes in biomass gain at forest-stand level, but insights into species-specific growth changes - that ultimately determine community-level responses - are lacking. Here, we analyse species-specific growth changes on a centennial scale, using growth data from tree-ring analysis for 13 tree species (~1300 trees), from three sites distributed across the tropics. We used an established (regional curve standardization) and a new (size-class isolation) growth-trend detection method and explicitly assessed the influence of biases on the trend detection. In addition, we assessed whether aggregated trends were present within and across study sites. We found evidence for decreasing growth rates over time for 8-10 species, whereas increases were noted for two species and one showed no trend. Additionally, we found evidence for weak aggregated growth decreases at the site in Thailand and when analysing all sites simultaneously. The observed growth reductions suggest deteriorating growth conditions, perhaps due to warming. However, other causes cannot be excluded, such as recovery from large-scale disturbances or changing forest dynamics. Our findings contrast growth patterns that would be expected if elevated CO2 would stimulate tree growth. These results suggest that commonly assumed growth increases of tropical forests may not occur, which could lead to erroneous predictions of carbon dynamics of tropical forest under climate change.

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.

Detecting long-term growth trends using tree rings: a critical evaluation of methods.

Tree-ring analysis is often used to assess long-term trends in tree growth. A variety of growth-trend detection methods (GDMs) exist to disentangle age/size trends in growth from long-term growth changes. However, these detrending methods strongly differ in approach, with possible implications for their output. Here, we critically evaluate the consistency, sensitivity, reliability and accuracy of four most widely used GDMs: conservative detrending (CD) applies mathematical functions to correct for decreasing ring widths with age; basal area correction (BAC) transforms diameter into basal area growth; regional curve standardization (RCS) detrends individual tree-ring series using average age/size trends; and size class isolation (SCI) calculates growth trends within separate size classes. First, we evaluated whether these GDMs produce consistent results applied to an empirical tree-ring data set of Melia azedarach, a tropical tree species from Thailand. Three GDMs yielded similar results - a growth decline over time - but the widely used CD method did not detect any change. Second, we assessed the sensitivity (probability of correct growth-trend detection), reliability (100% minus probability of detecting false trends) and accuracy (whether the strength of imposed trends is correctly detected) of these GDMs, by applying them to simulated growth trajectories with different imposed trends: no trend, strong trends (-6% and +6% change per decade) and weak trends (-2%, +2%). All methods except CD, showed high sensitivity, reliability and accuracy to detect strong imposed trends. However, these were considerably lower in the weak or no-trend scenarios. BAC showed good sensitivity and accuracy, but low reliability, indicating uncertainty of trend detection using this method. Our study reveals that the choice of GDM influences results of growth-trend studies. We recommend applying multiple methods when analysing trends and encourage performing sensitivity and reliability analysis. Finally, we recommend SCI and RCS, as these methods showed highest reliability to detect long-term growth trends.

Sapwood allocation in tropical trees: a test of hypotheses.

Carbon allocation to sapwood in tropical canopy trees is a key process determining forest carbon sequestration, and is at the heart of tree growth and dynamic global vegetation models (DGVM). Several allocation hypotheses exist including those applying assumptions on fixed allocation, pipe model, and hierarchical allocation between plant organs. We use a tree growth model (IBTREE) to evaluate these hypotheses by comparing simulated sapwood growth with 30 year tree ring records of the tropical long-lived tree Toona ciliata M. Roem. in Thailand. Simulated annual variation in wood production varied among hypotheses. Observed and simulated growth patterns matched most closely (r2=0.70) when hierarchical allocation was implemented, with low priority for sapwood. This allocation method showed realistic results with respect to reserve dynamics, partitioning and productivity and was the only one able to capture the large annual variation in tree ring width. Consequently, this method might also explain the large temporal variation in diameter growth and the occurrence of missing rings often encountered in other tropical tree species. Overall, our results show that sapwood growth is highly sensitive to allocation principles, and that allocation assumptions may greatly influence estimated carbon sequestration of tropical forests under climatic change.

Temperature and rainfall strongly drive temporal growth variation in Asian tropical forest trees.

Climate change effects on growth rates of tropical trees may lead to alterations in carbon cycling of carbon-rich tropical forests. However, climate sensitivity of broad-leaved lowland tropical trees is poorly understood. Dendrochronology (tree-ring analysis) provides a powerful tool to study the relationship between tropical tree growth and annual climate variability. We aimed to establish climate-growth relationships for five annual-ring forming tree species, using ring-width data from 459 canopy and understory trees from a seasonal tropical forest in western Thailand. Based on 183/459 trees, chronologies with total lengths between 29 and 62 years were produced for four out of five species. Bootstrapped correlation analysis revealed that climate-growth responses were similar among these four species. Growth was significantly negatively correlated with current-year maximum and minimum temperatures, and positively correlated with dry-season precipitation levels. Negative correlations between growth and temperature may be attributed to a positive relationship between temperature and autotrophic respiration rates. The positive relationship between growth and dry-season precipitation levels likely reflects the strong water demand during leaf flush. Mixed-effect models yielded results that were consistent across species: a negative effect of current wet-season maximum temperatures on growth, but also additive positive effects of, for example, prior dry-season maximum temperatures. Our analyses showed that annual growth variability in tropical trees is determined by a combination of both temperature and precipitation variability. With rising temperature, the predominantly negative relationship between temperature and growth may imply decreasing growth rates of tropical trees as a result of global warming.

Tropical forests and global change: filling knowledge gaps.

Tropical forests will experience major changes in environmental conditions this century. Understanding their responses to such changes is crucial to predicting global carbon cycling. Important knowledge gaps exist: the causes of recent changes in tropical forest dynamics remain unclear and the responses of entire tropical trees to environmental changes are poorly understood. In this Opinion article, we argue that filling these knowledge gaps requires a new research strategy, one that focuses on trees instead of leaves or communities, on long-term instead of short-term changes, and on understanding mechanisms instead of documenting changes. We propose the use of tree-ring analyses, stable-isotope analyses, manipulative field experiments, and well-validated simulation models to improve predictions of forest responses to global change.