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.

Lightning scars on tropical trees-Evidence and opportunities.

Lightning strikes are a significant cause of tree mortality and damage in some regions of the tropics. Formation of lightning scars on tropical trees, however, is considered rare and therefore of little relevance in identifying trees struck by lightning. Here, we suggest, based on observations made in the Bwindi Impenetrable National Park (Uganda), that lightning scars can be frequent and may be a useful diagnostic feature to aid in identifying trees struck by lightning.

Growth portfolios buffer climate-linked environmental change in marine systems.

Large-scale, climate-induced synchrony in the productivity of fish populations is becoming more pronounced in the world's oceans. As synchrony increases, a population's "portfolio" of responses can be diminished, in turn reducing its resilience to strong perturbation. Here we argue that the costs and benefits of trait synchronization, such as the expression of growth rate, are context dependent. Contrary to prevailing views, synchrony among individuals could actually be beneficial for populations if growth synchrony increases during favorable conditions, and then declines under poor conditions when a broader portfolio of responses could be useful. Importantly, growth synchrony among individuals within populations has seldom been measured, despite well-documented evidence of synchrony across populations. Here, we used century-scale time series of annual otolith growth to test for changes in growth synchronization among individuals within multiple populations of a marine keystone species (Atlantic cod, Gadus morhua). On the basis of 74,662 annual growth increments recorded in 13,749 otoliths, we detected a rising conformity in long-term growth rates within five northeast Atlantic cod populations in response to both favorable growth conditions and a large-scale, multidecadal mode of climate variability similar to the East Atlantic Pattern. The within-population synchrony was distinct from the across-population synchrony commonly reported for large-scale environmental drivers. Climate-linked, among-individual growth synchrony was also identified in other Northeast Atlantic pelagic, deep-sea and bivalve species. We hypothesize that growth synchrony in good years and growth asynchrony in poorer years reflects adaptive trait optimization and bet hedging, respectively, that could confer an unexpected, but pervasive and stabilizing, impact on marine population productivity in response to large-scale environmental change.

Biotic Indicators for Ecological State Change in Amazonian Floodplains.

Riverine floodplains are biologically diverse and productive ecosystems. Although tropical floodplains remain relatively conserved and ecologically functional compared to those at higher latitudes, they face accelerated hydropower development, climate change, and deforestation. Alterations to the flood pulse could act synergistically with other drivers of change to promote profound ecological state change at a large spatial scale. State change occurs when an ecosystem reaches a critical threshold or tipping point, which leads to an alternative qualitative state for the ecosystem. Visualizing an alternative state for Amazonian floodplains is not straightforward. Yet, it is critical to recognize that changes to the flood pulse could push tropical floodplain ecosystems over a tipping point with cascading adverse effects on biodiversity and ecosystem services. We characterize the Amazonian flood pulse regime, summarize evidence of flood pulse change, assess potential ecological repercussions, and provide a monitoring framework for tracking flood pulse change and detecting biotic responses.

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.

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.

The revolution of crossdating in marine palaeoecology and palaeoclimatology.

Over the past century, the dendrochronology technique of crossdating has been widely used to generate a global network of tree-ring chronologies that serves as a leading indicator of environmental variability and change. Only recently, however, has this same approach been applied to growth increments in calcified structures of bivalves, fish and corals in the world's oceans. As in trees, these crossdated marine chronologies are well replicated, annually resolved and absolutely dated, providing uninterrupted multi-decadal to millennial histories of ocean palaeoclimatic and palaeoecological processes. Moreover, they span an extensive geographical range, multiple trophic levels, habitats and functional types, and can be readily integrated with observational physical or biological records. Increment width is the most commonly measured parameter and reflects growth or productivity, though isotopic and elemental composition capture complementary aspects of environmental variability. As such, crossdated marine chronologies constitute powerful observational templates to establish climate-biology relationships, test hypotheses of ecosystem functioning, conduct multi-proxy reconstructions, provide constraints for numerical climate models, and evaluate the precise timing and nature of ocean-atmosphere interactions. These 'present-past-future' perspectives provide new insights into the mechanisms and feedbacks between the atmosphere and marine systems while providing indicators relevant to ecosystem-based approaches of fisheries management.

Rising synchrony controls western North American ecosystems.

Along the western margin of North America, the winter expression of the North Pacific High (NPH) strongly influences interannual variability in coastal upwelling, storm track position, precipitation, and river discharge. Coherence among these factors induces covariance among physical and biological processes across adjacent marine and terrestrial ecosystems. Here, we show that over the past century the degree and spatial extent of this covariance (synchrony) has substantially increased, and is coincident with rising variance in the winter NPH. Furthermore, centuries-long blue oak (Quercus douglasii) growth chronologies sensitive to the winter NPH provide robust evidence that modern levels of synchrony are among the highest observed in the context of the last 250 years. These trends may ultimately be linked to changing impacts of the El Niño Southern Oscillation on midlatitude ecosystems of North America. Such a rise in synchrony may destabilize ecosystems, expose populations to higher risks of extinction, and is thus a concern given the broad biological relevance of winter climate to biological systems.

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.

The value of crossdating to retain high-frequency variability, climate signals, and extreme events in environmental proxies.

High-resolution biogenic and geologic proxies in which one increment or layer is formed per year are crucial to describing natural ranges of environmental variability in Earth's physical and biological systems. However, dating controls are necessary to ensure temporal precision and accuracy; simple counts cannot ensure that all layers are placed correctly in time. Originally developed for tree-ring data, crossdating is the only such procedure that ensures all increments have been assigned the correct calendar year of formation. Here, we use growth-increment data from two tree species, two marine bivalve species, and a marine fish species to illustrate sensitivity of environmental signals to modest dating error rates. When falsely added or missed increments are induced at one and five percent rates, errors propagate back through time and eliminate high-frequency variability, climate signals, and evidence of extreme events while incorrectly dating and distorting major disturbances or other low-frequency processes. Our consecutive Monte Carlo experiments show that inaccuracies begin to accumulate in as little as two decades and can remove all but decadal-scale processes after as little as two centuries. Real-world scenarios may have even greater consequence in the absence of crossdating. Given this sensitivity to signal loss, the fundamental tenets of crossdating must be applied to fully resolve environmental signals, a point we underscore as the frontiers of growth-increment analysis continue to expand into tropical, freshwater, and marine environments.

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.

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.