Leaf gene expression trajectories during the growing season are consistent between sites and years in American beech.

Transcriptomics provides a versatile tool for ecological monitoring. Here, through genome-guided profiling of transcripts mapping to 33 042 gene models, expression differences can be discerned among multi-year and seasonal leaf samples collected from American beech trees at two latitudinally separated sites. Despite a bottleneck due to post-Columbian deforestation, the single nucleotide polymorphism-based population genetic background analysis has yielded sufficient variation to account for differences between populations and among individuals. Our expression analyses during spring-summer and summer-autumn transitions for two consecutive years involved 4197 differentially expressed protein coding genes. Using Populus orthologues we reconstructed a protein-protein interactome representing leaf physiological states of trees during the seasonal transitions. Gene set enrichment analysis revealed gene ontology terms that highlight molecular functions and biological processes possibly influenced by abiotic forcings such as recovery from drought and response to excess precipitation. Further, based on 324 co-regulated transcripts, we focused on a subset of GO terms that could be putatively attributed to late spring phenological shifts. Our conservative results indicate that extended transcriptome-based monitoring of forests can capture diverse ranges of responses including air quality, chronic disease, as well as herbivore outbreaks that require activation and/or downregulation of genes collectively tuning reaction norms maintaining the survival of long living trees such as the American beech.

Latitudinal patterns in stabilizing density dependence of forest communities.

Numerous studies have shown reduced performance in plants that are surrounded by neighbours of the same species1,2, a phenomenon known as conspecific negative density dependence (CNDD)3. A long-held ecological hypothesis posits that CNDD is more pronounced in tropical than in temperate forests4,5, which increases community stabilization, species coexistence and the diversity of local tree species6,7. Previous analyses supporting such a latitudinal gradient in CNDD8,9 have suffered from methodological limitations related to the use of static data10-12. Here we present a comprehensive assessment of latitudinal CNDD patterns using dynamic mortality data to estimate species-site-specific CNDD across 23 sites. Averaged across species, we found that stabilizing CNDD was present at all except one site, but that average stabilizing CNDD was not stronger toward the tropics. However, in tropical tree communities, rare and intermediate abundant species experienced stronger stabilizing CNDD than did common species. This pattern was absent in temperate forests, which suggests that CNDD influences species abundances more strongly in tropical forests than it does in temperate ones13. We also found that interspecific variation in CNDD, which might attenuate its stabilizing effect on species diversity14,15, was high but not significantly different across latitudes. Although the consequences of these patterns for latitudinal diversity gradients are difficult to evaluate, we speculate that a more effective regulation of population abundances could translate into greater stabilization of tropical tree communities and thus contribute to the high local diversity of tropical forests.

Tropical tree ectomycorrhiza are distributed independently of soil nutrients.

Mycorrhizae, a form of plant-fungal symbioses, mediate vegetation impacts on ecosystem functioning. Climatic effects on decomposition and soil quality are suggested to drive mycorrhizal distributions, with arbuscular mycorrhizal plants prevailing in low-latitude/high-soil-quality areas and ectomycorrhizal (EcM) plants in high-latitude/low-soil-quality areas. However, these generalizations, based on coarse-resolution data, obscure finer-scale variations and result in high uncertainties in the predicted distributions of mycorrhizal types and their drivers. Using data from 31 lowland tropical forests, both at a coarse scale (mean-plot-level data) and fine scale (20 × 20 metres from a subset of 16 sites), we demonstrate that the distribution and abundance of EcM-associated trees are independent of soil quality. Resource exchange differences among mycorrhizal partners, stemming from diverse evolutionary origins of mycorrhizal fungi, may decouple soil fertility from the advantage provided by mycorrhizal associations. Additionally, distinct historical biogeographies and diversification patterns have led to differences in forest composition and nutrient-acquisition strategies across three major tropical regions. Notably, Africa and Asia's lowland tropical forests have abundant EcM trees, whereas they are relatively scarce in lowland neotropical forests. A greater understanding of the functional biology of mycorrhizal symbiosis is required, especially in the lowland tropics, to overcome biases from assuming similarity to temperate and boreal regions.

Damage to living trees contributes to almost half of the biomass losses in tropical forests.

Accurate estimates of forest biomass stocks and fluxes are needed to quantify global carbon budgets and assess the response of forests to climate change. However, most forest inventories consider tree mortality as the only aboveground biomass (AGB) loss without accounting for losses via damage to living trees: branchfall, trunk breakage, and wood decay. Here, we use ~151,000 annual records of tree survival and structural completeness to compare AGB loss via damage to living trees to total AGB loss (mortality + damage) in seven tropical forests widely distributed across environmental conditions. We find that 42% (3.62 Mg ha-1 year-1 ; 95% confidence interval [CI] 2.36-5.25) of total AGB loss (8.72 Mg ha-1 year-1 ; CI 5.57-12.86) is due to damage to living trees. Total AGB loss was highly variable among forests, but these differences were mainly caused by site variability in damage-related AGB losses rather than by mortality-related AGB losses. We show that conventional forest inventories overestimate stand-level AGB stocks by 4% (1%-17% range across forests) because assume structurally complete trees, underestimate total AGB loss by 29% (6%-57% range across forests) due to overlooked damage-related AGB losses, and overestimate AGB loss via mortality by 22% (7%-80% range across forests) because of the assumption that trees are undamaged before dying. Our results indicate that forest carbon fluxes are higher than previously thought. Damage on living trees is an underappreciated component of the forest carbon cycle that is likely to become even more important as the frequency and severity of forest disturbances increase.

Toward a forest biomass reference measurement system for remote sensing applications.

Forests contribute to climate change mitigation through carbon storage and uptake, but the extent to which this carbon pool varies in space and time is still poorly known. Several Earth Observation missions have been specifically designed to address this issue, for example, NASA's GEDI, NASA-ISRO's NISAR and ESA's BIOMASS. Yet, all these missions' products require independent and consistent validation. A permanent, global, in situ, site-based forest biomass reference measurement system relying on ground data of the highest possible quality is therefore needed. Here, we have assembled a list of almost 200 high-quality sites through an in-depth review of the literature and expert knowledge. In this study, we explore how representative these sites are in terms of their coverage of environmental conditions, geographical space and biomass-related forest structure, compared to those experienced by forests worldwide. This work also aims at identifying which sites are the most representative, and where to invest to improve the representativeness of the proposed system. We show that the environmental coverage of the system does not seem to improve after at least the 175 most representative sites are included, but geographical and structural coverages continue to improve as more sites are added. We highlight the areas of poor environmental, geographical, or structural coverage, including, but not limited to, Canada, the western half of the USA, Mexico, Patagonia, Angola, Zambia, eastern Russia, and tropical and subtropical highlands (e.g. in Colombia, the Himalayas, Borneo, Papua). For the proposed system to succeed, we stress that (1) data must be collected and processed applying the same standards across all countries and continents; (2) system establishment and management must be inclusive and equitable, with careful consideration of working conditions; and (3) training and site partner involvement in downstream activities should be mandatory.

Community phylogeny and spatial scale affect phylogenetic diversity metrics in a species-rich rainforest in Borneo.

Community phylogenetic analysis is an effective approach to understanding the process of community formation. The phylogenetic tree of the species pool is reconstructed in the first step, and the phylogenetic tree obtained in the second step is used to analyze phylogenetic diversity. Sythetic trees have often been used in the construction of phylogenentic trees; however, in tropical rainforests with many closely related species, synthetic trees contain many unresolved nodes, which may affect the results of phylogenetic structure analysis. Here, we constructed a phylogenetic tree using DNA barcode sequences (rbcL, matK, trnH-psbA) for 737 tree species from the rainforests of Borneo, which have a high-species diversity and many closely related species. The phylogenetic tree had fewer polytomies and more branch length variations than the Phylocom synthetic trees. Comparison of community phylogenetic analyses indicated that values of the standardized effect size of mean pairwise distance (SES-MPD) were highly correlated between Phylocom and DNA barcode trees, but less so for the standardized effect size of mean nearest taxon distance (SES-MNTD), suggesting that caution is needed when using synthetic trees for communities containing many congeneric species, especially when using SES-MNTD. Simulation analysis suggested that spatial dependence on phylogenetic diversity is related to the phylogenetic signal of the species' habitat niche and the spatial structure of habitat, indicating the importance of detailed phylogeny in understanding community assembly processes.

Comparative transcriptomics of tropical woody plants supports fast and furious strategy along the leaf economics spectrum in lianas.

Lianas, climbing woody plants, influence the structure and function of tropical forests. Climbing traits have evolved multiple times, including ancestral groups such as gymnosperms and pteridophytes, but the genetic basis of the liana strategy is largely unknown. Here, we use a comparative transcriptomic approach for 47 tropical plant species, including ten lianas of diverse taxonomic origins, to identify genes that are consistently expressed or downregulated only in lianas. Our comparative analysis of full-length transcripts enabled the identification of a core interactomic network common to lianas. Sets of transcripts identified from our analysis reveal features related to functional traits pertinent to leaf economics spectrum in lianas, include upregulation of genes controlling epidermal cuticular properties, cell wall remodeling, carbon concentrating mechanism, cell cycle progression, DNA repair and a large suit of downregulated transcription factors and enzymes involved in ABA-mediated stress response as well as lignin and suberin synthesis. All together, these genes are known to be significant in shaping plant morphologies through responses such as gravitropism, phyllotaxy and shade avoidance.

Tree crown damage and its effects on forest carbon cycling in a tropical forest.

Crown damage can account for over 23% of canopy biomass turnover in tropical forests and is a strong predictor of tree mortality; yet, it is not typically represented in vegetation models. We incorporate crown damage into the Functionally Assembled Terrestrial Ecosystem Simulator (FATES), to evaluate how lags between damage and tree recovery or death alter demographic rates and patterns of carbon turnover. We represent crown damage as a reduction in a tree's crown area and leaf and branch biomass, and allow associated variation in the ratio of aboveground to belowground plant tissue. We compare simulations with crown damage to simulations with equivalent instant increases in mortality and benchmark results against data from Barro Colorado Island (BCI), Panama. In FATES, crown damage causes decreases in growth rates that match observations from BCI. Crown damage leads to increases in carbon starvation mortality in FATES, but only in configurations with high root respiration and decreases in carbon storage following damage. Crown damage also alters competitive dynamics, as plant functional types that can recover from crown damage outcompete those that cannot. This is a first exploration of the trade-off between the additional complexity of the novel crown damage module and improved predictive capabilities. At BCI, a tropical forest that does not experience high levels of disturbance, both the crown damage simulations and simulations with equivalent increases in mortality does a reasonable job of capturing observations. The crown damage module provides functionality for exploring dynamics in forests with more extreme disturbances such as cyclones and for capturing the synergistic effects of disturbances that overlap in space and time.

Distribution of biomass dynamics in relation to tree size in forests across the world.

Tree size shapes forest carbon dynamics and determines how trees interact with their environment, including a changing climate. Here, we conduct the first global analysis of among-site differences in how aboveground biomass stocks and fluxes are distributed with tree size. We analyzed repeat tree censuses from 25 large-scale (4-52 ha) forest plots spanning a broad climatic range over five continents to characterize how aboveground biomass, woody productivity, and woody mortality vary with tree diameter. We examined how the median, dispersion, and skewness of these size-related distributions vary with mean annual temperature and precipitation. In warmer forests, aboveground biomass, woody productivity, and woody mortality were more broadly distributed with respect to tree size. In warmer and wetter forests, aboveground biomass and woody productivity were more right skewed, with a long tail towards large trees. Small trees (1-10 cm diameter) contributed more to productivity and mortality than to biomass, highlighting the importance of including these trees in analyses of forest dynamics. Our findings provide an improved characterization of climate-driven forest differences in the size structure of aboveground biomass and dynamics of that biomass, as well as refined benchmarks for capturing climate influences in vegetation demographic models.

Demographic composition, not demographic diversity, predicts biomass and turnover across temperate and tropical forests.

The growth and survival of individual trees determine the physical structure of a forest with important consequences for forest function. However, given the diversity of tree species and forest biomes, quantifying the multitude of demographic strategies within and across forests and the way that they translate into forest structure and function remains a significant challenge. Here, we quantify the demographic rates of 1961 tree species from temperate and tropical forests and evaluate how demographic diversity (DD) and demographic composition (DC) differ across forests, and how these differences in demography relate to species richness, aboveground biomass (AGB), and carbon residence time. We find wide variation in DD and DC across forest plots, patterns that are not explained by species richness or climate variables alone. There is no evidence that DD has an effect on either AGB or carbon residence time. Rather, the DC of forests, specifically the relative abundance of large statured species, predicted both biomass and carbon residence time. Our results demonstrate the distinct DCs of globally distributed forests, reflecting biogeography, recent history, and current plot conditions. Linking the DC of forests to resilience or vulnerability to climate change, will improve the precision and accuracy of predictions of future forest composition, structure, and function.

Individual tree damage dominates mortality risk factors across six tropical forests.

The relative importance of tree mortality risk factors remains unknown, especially in diverse tropical forests where species may vary widely in their responses to particular conditions. We present a new framework for quantifying the importance of mortality risk factors and apply it to compare 19 risks on 31 203 trees (1977 species) in 14 one-year periods in six tropical forests. We defined a condition as a risk factor for a species if it was associated with at least a doubling of mortality rate in univariate analyses. For each risk, we estimated prevalence (frequency), lethality (difference in mortality between trees with and without the risk) and impact ('excess mortality' associated with the risk, relative to stand-level mortality). The most impactful risk factors were light limitation and crown/trunk loss; the most prevalent were light limitation and small size; the most lethal were leaf damage and wounds. Modes of death (standing, broken and uprooted) had limited links with previous conditions and mortality risk factors. We provide the first ranking of importance of tree-level mortality risk factors in tropical forests. Future research should focus on the links between these risks, their climatic drivers and the physiological processes to enable mechanistic predictions of future tree mortality.

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.

Arbuscular mycorrhizal trees influence the latitudinal beta-diversity gradient of tree communities in forests worldwide.

Arbuscular mycorrhizal (AM) and ectomycorrhizal (EcM) associations are critical for host-tree performance. However, how mycorrhizal associations correlate with the latitudinal tree beta-diversity remains untested. Using a global dataset of 45 forest plots representing 2,804,270 trees across 3840 species, we test how AM and EcM trees contribute to total beta-diversity and its components (turnover and nestedness) of all trees. We find AM rather than EcM trees predominantly contribute to decreasing total beta-diversity and turnover and increasing nestedness with increasing latitude, probably because wide distributions of EcM trees do not generate strong compositional differences among localities. Environmental variables, especially temperature and precipitation, are strongly correlated with beta-diversity patterns for both AM trees and all trees rather than EcM trees. Results support our hypotheses that latitudinal beta-diversity patterns and environmental effects on these patterns are highly dependent on mycorrhizal types. Our findings highlight the importance of AM-dominated forests for conserving global forest biodiversity.

Consequences of spatial patterns for coexistence in species-rich plant communities.

Ecology cannot yet fully explain why so many tree species coexist in natural communities such as tropical forests. A major difficulty is linking individual-level processes to community dynamics. We propose a combination of tree spatial data, spatial statistics and dynamical theory to reveal the relationship between spatial patterns and population-level interaction coefficients and their consequences for multispecies dynamics and coexistence. Here we show that the emerging population-level interaction coefficients have, for a broad range of circumstances, a simpler structure than their individual-level counterparts, which allows for an analytical treatment of equilibrium and stability conditions. Mechanisms such as animal seed dispersal, which result in clustering of recruits that is decoupled from parent locations, lead to a rare-species advantage and coexistence of otherwise neutral competitors. Linking spatial statistics with theories of community dynamics offers new avenues for explaining species coexistence and calls for rethinking community ecology through a spatial lens.

Wildlife disturbances as a source of conspecific negative density-dependent mortality in tropical trees.

Large vertebrates are rarely considered important drivers of conspecific negative density-dependent mortality (CNDD) in plants because they are generalist consumers. However, disturbances like trampling and nesting also cause plant mortality, and their impact on plant diversity depends on the spatial overlap between wildlife habitat preferences and plant species composition. We studied the impact of native wildlife on a hyperdiverse tree community in Malaysia. Pigs (Sus scrofa) are abnormally abundant at the site due to food subsidies in nearby farmland and they construct birthing nests using hundreds of tree saplings. We tagged 34 950 tree saplings in a 25 ha plot during an initial census and assessed the source mortality by recovering tree tags from pig nests (n = 1672 pig-induced deaths). At the stand scale, pigs nested in flat dry habitats, and at the local neighbourhood scale, they nested within clumps of saplings, both of which are intuitive for safe and efficient nest building. At the stand scale, flat dry habitats contained higher sapling densities and higher proportions of common species, so pig nesting increased the weighted average species evenness across habitats. At the neighbourhood scale, pig-induced sapling mortality was associated with higher heterospecific and especially conspecific sapling densities. Tree species have clumped distributions due to dispersal limitation and habitat filtering, so pig disturbances in sapling clumps indirectly caused CNDD. As a result, Pielou species evenness in 400 m2 quadrats increased 105% more in areas with pig-induced deaths than areas without disturbances. Wildlife induced CNDD and this supported tree species evenness, but they also drove a 62% decline in sapling densities from 1996 to 2010, which is unsustainable. We suspect pig nesting is an important feature shaping tree composition throughout the region.

Leaf turgor loss point shapes local and regional distributions of evergreen but not deciduous tropical trees.

The effects of climate change on tropical forests will depend on how diverse tropical tree species respond to drought. Current distributions of evergreen and deciduous tree species across local and regional moisture gradients reflect their ability to tolerate drought stress, and might be explained by functional traits. We measured leaf water potential at turgor loss (i.e. 'wilting point'; πtlp ), wood density (WD) and leaf mass per area (LMA) on 50 of the most abundant tree species in central Panama. We then tested their ability to explain distributions of evergreen and deciduous species within a 50 ha plot on Barro Colorado Island and across a 70 km rainfall gradient spanning the Isthmus of Panama. Among evergreen trees, species with lower πtlp were associated with drier habitats, with πtlp explaining 28% and 32% of habitat association on local and regional scales, respectively, greatly exceeding the predictive power of WD and LMA. In contrast, πtlp did not predict habitat associations among deciduous species. Across spatial scales, πtlp is a useful indicator of habitat preference for tropical tree species that retain their leaves during periods of water stress, and holds the potential to predict vegetation responses to climate change.

The interspecific growth-mortality trade-off is not a general framework for tropical forest community structure.

Resource allocation within trees is a zero-sum game. Unavoidable trade-offs dictate that allocation to growth-promoting functions curtails other functions, generating a gradient of investment in growth versus survival along which tree species align, known as the interspecific growth-mortality trade-off. This paradigm is widely accepted but not well established. Using demographic data for 1,111 tree species across ten tropical forests, we tested the generality of the growth-mortality trade-off and evaluated its underlying drivers using two species-specific parameters describing resource allocation strategies: tolerance of resource limitation and responsiveness of allocation to resource access. Globally, a canonical growth-mortality trade-off emerged, but the trade-off was strongly observed only in less disturbance-prone forests, which contained diverse resource allocation strategies. Only half of disturbance-prone forests, which lacked tolerant species, exhibited the trade-off. Supported by a theoretical model, our findings raise questions about whether the growth-mortality trade-off is a universally applicable organizing framework for understanding tropical forest community structure.

Soil nitrogen concentration mediates the relationship between leguminous trees and neighbor diversity in tropical forests.

Legumes provide an essential service to ecosystems by capturing nitrogen from the atmosphere and delivering it to the soil, where it may then be available to other plants. However, this facilitation by legumes has not been widely studied in global tropical forests. Demographic data from 11 large forest plots (16-60 ha) ranging from 5.25° S to 29.25° N latitude show that within forests, leguminous trees have a larger effect on neighbor diversity than non-legumes. Where soil nitrogen is high, most legume species have higher neighbor diversity than non-legumes. Where soil nitrogen is low, most legumes have lower neighbor diversity than non-legumes. No facilitation effect on neighbor basal area was observed in either high or low soil N conditions. The legume-soil nitrogen positive feedback that promotes tree diversity has both theoretical implications for understanding species coexistence in diverse forests, and practical implications for the utilization of legumes in forest restoration.

Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest.

Arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) produce contrasting plant-soil feedbacks, but how these feedbacks are constrained by lithology is poorly understood. We investigated the hypothesis that lithological drivers of soil fertility filter plant resource economic strategies in ways that influence the relative fitness of trees with AMF or EMF symbioses in a Bornean rain forest containing species with both mycorrhizal strategies. Using forest inventory data on 1245 tree species, we found that although AMF-hosting trees had greater relative dominance on all soil types, with declining lithological soil fertility EMF-hosting trees became more dominant. Data on 13 leaf traits and wood density for a total of 150 species showed that variation was almost always associated with soil type, whereas for six leaf traits (structural properties; carbon, nitrogen, phosphorus ratios, nitrogen isotopes), variation was also associated with mycorrhizal strategy. EMF-hosting species had slower leaf economics than AMF-hosts, demonstrating the central role of mycorrhizal symbiosis in plant resource economies. At the global scale, climate has been shown to shape forest mycorrhizal composition, but here we show that in communities it depends on soil lithology, suggesting scale-dependent abiotic factors influence feedbacks underlying the relative fitness of different mycorrhizal strategies.