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.

Intraspecific alternative phenotypes contribute to variation in species' strategies for growth.

Ecologists have historically sought to identify the mechanisms underlying the maintenance of local species diversity. High-dimensional trait-based relationships, such as alternative phenotypes, have been hypothesized as important for maintaining species diversity such that phenotypically dissimilar individuals compete less for resources but have similar performance in a given environment. The presence of alternative phenotypes has primarily been investigated at the community level, despite the importance of intraspecific variation to diversity maintenance. The aims of this research are to (1) determine the presence or absence of intraspecific alternative phenotypes in three species of tropical tree seedlings, (2) investigate if these different species use the same alternative phenotypes for growth success, and (3) evaluate how findings align with species co-occurrence patterns. We model species-specific relative growth rate with individual-level measurements of leaf mass per area (LMA) and root mass fraction (RMF), environmental data, and their interactions. We find that two of the three species have intraspecific alternative phenotypes, with individuals within species having different functional forms leading to similar growth. Interestingly, individuals within these species use the same trait combinations, high LMA × low RMF and low LMA × high RMF, in high soil nutrient environments to acquire resources for higher growth. This similarity among species in intraspecific alternative phenotypes and variables that contribute most to growth may lead to their negative spatial co-occurrence. Overall, we find that multiple traits or interactions between traits and the environment drive species-specific strategies for growth, but that individuals within species leverage this multi-dimensionality in different ways for growth success.

Biogeographic context is related to local scale tree demography, co-occurrence and functional differentiation.

Identifying the drivers of community structure and dynamics is a major pursuit in ecology. Emphasis is typically placed on the importance of local scale interactions when attempting to explain these fundamental ecological patterns. However, regional scale phenomena are also important predictors. The importance of regional scale context should be more evident in assemblages where multiple species are close to their range margins. Here, we test the importance of regional scale context using data from a temperate forest plot that contains two species groups - one near its northern range limit and one near its southern range limit. We show the proximity of species to their southern or northern range margins is linked to local scale co-occurrence, similarity in gene expression responses to a key environmental driver, demographic performance and inter-specific variation in conspecific negative density dependence. In sum, many of the key local scale patterns and processes of interest to community ecologists are linked to biogeographic context that is frequently ignored.

Phytochemical diversity impacts herbivory in a tropical rainforest tree community.

Metabolomics provides an unprecedented window into diverse plant secondary metabolites that represent a potentially critical niche dimension in tropical forests underlying species coexistence. Here, we used untargeted metabolomics to evaluate chemical composition of 358 tree species and its relationship with phylogeny and variation in light environment, soil nutrients, and insect herbivore leaf damage in a tropical rainforest plot. We report no phylogenetic signal in most compound classes, indicating rapid diversification in tree metabolomes. We found that locally co-occurring species were more chemically dissimilar than random and that local chemical dispersion and metabolite diversity were associated with lower herbivory, especially that of specialist insect herbivores. Our results highlight the role of secondary metabolites in mediating plant-herbivore interactions and their potential to facilitate niche differentiation in a manner that contributes to species coexistence. Furthermore, our findings suggest that specialist herbivore pressure is an important mechanism promoting phytochemical diversity in tropical forests.

Demographic trade-offs and functional shifts in a hurricane-impacted tropical forest.

BACKGROUND AND AIMS: Understanding shifts in the demographic and functional composition of forests after major natural disturbances has become increasingly relevant given the accelerating rates of climate change and elevated frequency of natural disturbances. Although plant demographic strategies are often described across a slow-fast continuum, severe and frequent disturbance events influencing demographic processes may alter the demographic trade-offs and the functional composition of forests. We examined demographic trade-offs and the shifts in functional traits in a hurricane-disturbed forest using long-term data from the Luquillo Forest Dynamics Plot (LFPD) in Puerto Rico. METHODS: We analysed information on growth, survival, seed rain and seedling recruitment for 30 woody species in the LFDP. In addition, we compiled data on leaf, seed and wood functional traits that capture the main ecological strategies for plants. We used this information to identify the main axes of demographic variation for this forest community and evaluate shifts in community-weighted means for traits from 2000 to 2016. KEY RESULTS: The previously identified growth-survival trade-off was not observed. Instead, we identified a fecundity-growth trade-off and an axis representing seedling-to-adult survival. Both axes formed dimensions independent of resprouting ability. Also, changes in tree species composition during the post-hurricane period reflected a directional shift from seedling and tree communities dominated by acquisitive towards conservative leaf economics traits and large seed mass. Wood specific gravity, however, did not show significant directional changes over time. CONCLUSIONS: Our study demonstrates that tree demographic strategies coping with frequent storms and hurricane disturbances deviate from strategies typically observed in undisturbed forests, yet the shifts in functional composition still conform to the expected changes from acquisitive to conservative resource-uptake strategies expected over succession. In the face of increased rates of natural and anthropogenic disturbance in tropical regions, our results anticipate shifts in species demographic trade-offs and different functional dimensions.

Plant functional traits have globally consistent effects on competition.

Phenotypic traits and their associated trade-offs have been shown to have globally consistent effects on individual plant physiological functions, but how these effects scale up to influence competition, a key driver of community assembly in terrestrial vegetation, has remained unclear. Here we use growth data from more than 3 million trees in over 140,000 plots across the world to show how three key functional traits--wood density, specific leaf area and maximum height--consistently influence competitive interactions. Fast maximum growth of a species was correlated negatively with its wood density in all biomes, and positively with its specific leaf area in most biomes. Low wood density was also correlated with a low ability to tolerate competition and a low competitive effect on neighbours, while high specific leaf area was correlated with a low competitive effect. Thus, traits generate trade-offs between performance with competition versus performance without competition, a fundamental ingredient in the classical hypothesis that the coexistence of plant species is enabled via differentiation in their successional strategies. Competition within species was stronger than between species, but an increase in trait dissimilarity between species had little influence in weakening competition. No benefit of dissimilarity was detected for specific leaf area or wood density, and only a weak benefit for maximum height. Our trait-based approach to modelling competition makes generalization possible across the forest ecosystems of the world and their highly diverse species composition.

Climate shapes and shifts functional biodiversity in forests worldwide.

Much ecological research aims to explain how climate impacts biodiversity and ecosystem-level processes through functional traits that link environment with individual performance. However, the specific climatic drivers of functional diversity across space and time remain unclear due largely to limitations in the availability of paired trait and climate data. We compile and analyze a global forest dataset using a method based on abundance-weighted trait moments to assess how climate influences the shapes of whole-community trait distributions. Our approach combines abundance-weighted metrics with diverse climate factors to produce a comprehensive catalog of trait-climate relationships that differ dramatically-27% of significant results change in sign and 71% disagree on sign, significance, or both-from traditional species-weighted methods. We find that (i) functional diversity generally declines with increasing latitude and elevation, (ii) temperature variability and vapor pressure are the strongest drivers of geographic shifts in functional composition and ecological strategies, and (iii) functional composition may currently be shifting over time due to rapid climate warming. Our analysis demonstrates that climate strongly governs functional diversity and provides essential information needed to predict how biodiversity and ecosystem function will respond to climate change.

On the modelling of tropical tree growth: the importance of intra-specific trait variation, non-linear functions and phenotypic integration.

BACKGROUND AND AIMS: The composition and dynamics of plant communities arise from individual-level demographic outcomes, which are driven by interactions between phenotypes and the environment. Functional traits that can be measured across plants are frequently used to model plant growth and survival. Perhaps surprisingly, species average trait values are often used in these studies and, in some cases, these trait values come from other regions or averages calculated from global databases. This data aggregation potentially results in a large loss of valuable information that probably results in models of plant performance that are weak or even misleading. METHODS: We present individual-level trait and fine-scale growth data from >500 co-occurring individual trees from 20 species in a Chinese tropical rain forest. We construct Bayesian models of growth informed by theory and construct hierarchical Bayesian models that utilize both individual- and species-level trait data, and compare these models with models only using individual-level data. KEY RESULTS: We show that trait-growth relationships measured at the individual level vary across species, are often weak using commonly measured traits and do not align with the results of analyses conducted at the species level. However, when we construct individual-level models of growth using leaf area ratio approximations and integrated phenotypes, we generated strong predictive models of tree growth. CONCLUSIONS: Here, we have shown that individual-level models of tree growth that are built using integrative traits always outperform individual-level models of tree growth that use commonly measured traits. Furthermore, individual-level models, generally, do not support the findings of trait-growth relationships quantified at the species level. This indicates that aggregating trait and growth data to the species level results in poorer and probably misleading models of how traits are related to tree performance.

Three keys to the radiation of angiosperms into freezing environments.

Early flowering plants are thought to have been woody species restricted to warm habitats. This lineage has since radiated into almost every climate, with manifold growth forms. As angiosperms spread and climate changed, they evolved mechanisms to cope with episodic freezing. To explore the evolution of traits underpinning the ability to persist in freezing conditions, we assembled a large species-level database of growth habit (woody or herbaceous; 49,064 species), as well as leaf phenology (evergreen or deciduous), diameter of hydraulic conduits (that is, xylem vessels and tracheids) and climate occupancies (exposure to freezing). To model the evolution of species' traits and climate occupancies, we combined these data with an unparalleled dated molecular phylogeny (32,223 species) for land plants. Here we show that woody clades successfully moved into freezing-prone environments by either possessing transport networks of small safe conduits and/or shutting down hydraulic function by dropping leaves during freezing. Herbaceous species largely avoided freezing periods by senescing cheaply constructed aboveground tissue. Growth habit has long been considered labile, but we find that growth habit was less labile than climate occupancy. Additionally, freezing environments were largely filled by lineages that had already become herbs or, when remaining woody, already had small conduits (that is, the trait evolved before the climate occupancy). By contrast, most deciduous woody lineages had an evolutionary shift to seasonally shedding their leaves only after exposure to freezing (that is, the climate occupancy evolved before the trait). For angiosperms to inhabit novel cold environments they had to gain new structural and functional trait solutions; our results suggest that many of these solutions were probably acquired before their foray into the cold.

Dry conditions and disturbance promote liana seedling survival and abundance.

Species composition and community structure in Neotropical forests have been severely affected by increases in climate change and disturbance. Among the most conspicuous changes is the proliferation of lianas. These increases have affected not only the carbon storage capacity of forests but also tree dynamics by reducing tree growth and increasing mortality. Despite the importance of lianas in Neotropical forests, most of the studies on lianas have focused on adult stages, ignoring dynamics at the seedlings stage. Here, we asked whether observed increases in liana abundance are associated with a demographic advantage that emerges early in liana ontogeny and with decreased precipitation and increased disturbance. To test this, we compared patterns of growth and survival between liana seedlings and tree seedlings using a long-term data set of seedling plots from a subtropical wet forest in Puerto Rico, USA. Then, we examined the effect of precipitation and land use history on these demographic variables. We found evidence for liana seedling survival advantage over trees, but no growth advantages. This survival advantage exhibited significant temporal variation linked with patterns of rainfall, as well as differences associated with land-use history in the study area. Furthermore, we found that neighborhood density has a negative effect on liana survival and growth. Our results indicate that liana proliferation is likely related to a survival advantage that emerges in early stages and is influenced by climatic conditions and past disturbance. Predicted climatic changes in rainfall patterns, including more frequent and severe droughts, together with increases in disturbance, could have a significant effect on seedling tropical communities by favoring lianas.

Intraspecific variation in traits and tree growth along an elevational gradient in a subtropical forest.

A conspicuous feature of natural communities is that individuals within species exhibit broad variation in their phenotype. While the phenotypic differences among species are prominent and have received considerable attention in earlier studies, recent findings suggest that about 40% of the trait variation is found within species. How this intraspecific variation is related to underlying environmental gradients and ultimately linked to performance is an outstanding question in ecology and evolution. Here, we study six broadly distributed species across an elevational gradient in a subtropical forest. We focused on five functional traits reflecting plant functional differentiation in stem transport, leaf architecture, and leaf resource acquisition. We found that leaf thickness, leaf toughness, and specific leaf area generally varied with elevation, while wood density and leaf area exhibited constrained variation. Results on multivariate trait axes also showed mixed evidence with the PC1 values (positively related to leaf toughness and negatively related to specific leaf area) shifting with elevation, while PC2 values (negatively related to wood density) did not change with elevation. We also found that, despite the important variation in some traits along the gradient, growth performance did not follow this same trend. This suggests that strong directional changes in traits along the gradient may result in similar levels of demographic performance. The results, therefore, challenge the simple expectation that a trait will correlate with a demographic rate. More nuanced approaches and additional mechanisms must be considered to advance understanding of the performance-trait relationships.

Precipitation mediates sap flux sensitivity to evaporative demand in the neotropics.

Transpiration in humid tropical forests modulates the global water cycle and is a key driver of climate regulation. Yet, our understanding of how tropical trees regulate sap flux in response to climate variability remains elusive. With a progressively warming climate, atmospheric evaporative demand [i.e., vapor pressure deficit (VPD)] will be increasingly important for plant functioning, becoming the major control of plant water use in the twenty-first century. Using measurements in 34 tree species at seven sites across a precipitation gradient in the neotropics, we determined how the maximum sap flux velocity (vmax) and the VPD threshold at which vmax is reached (VPDmax) vary with precipitation regime [mean annual precipitation (MAP); seasonal drought intensity (PDRY)] and two functional traits related to foliar and wood economics spectra [leaf mass per area (LMA); wood specific gravity (WSG)]. We show that, even though vmax is highly variable within sites, it follows a negative trend in response to increasing MAP and PDRY across sites. LMA and WSG exerted little effect on vmax and VPDmax, suggesting that these widely used functional traits provide limited explanatory power of dynamic plant responses to environmental variation within hyper-diverse forests. This study demonstrates that long-term precipitation plays an important role in the sap flux response of humid tropical forests to VPD. Our findings suggest that under higher evaporative demand, trees growing in wetter environments in humid tropical regions may be subjected to reduced water exchange with the atmosphere relative to trees growing in drier climates.

Intra-specific relatedness, spatial clustering and reduced demographic performance in tropical rainforest trees.

Intra-specific negative density dependence promotes species coexistence by regulating population sizes. Patterns consistent with such density dependence are frequently reported in diverse tropical tree communities. Empirical evidence demonstrating whether intra-specific variation is related to these patterns, however, is lacking. The present study addresses this important knowledge gap by genotyping all individuals of a tropical tree in a long-term forest dynamics plot in tropical China. We show that related individuals are often spatially clustered, but having closely related neighbours reduces the growth performance of focal trees. We infer from the evidence that dispersal limitation and negative density dependence are operating simultaneously to impact the spatial distributions of genotypes in a natural population. Furthermore, dispersal limitation decreases local intra-specific genetic diversity and increases negative density dependence thereby promoting niche differences and species coexistence as predicted by theory.

Associations among arbuscular mycorrhizal fungi and seedlings are predicted to change with tree successional status.

Arbuscular mycorrhizal (AM) fungi in the soil may influence tropical tree dynamics and forest succession. The mechanisms are poorly understood, because the functional characteristics and abundances of tree species and AM fungi are likely to be codependent. We used generalized joint attribute modeling to evaluate if AM fungi are associated with three forest community metrics for a sub-tropical montane forest in Puerto Rico. The metrics chosen to reflect changes during forest succession are the abundance of seedlings of different successional status, the amount of foliar damage on seedlings of different successional status, and community-weighted mean functional trait values (adult specific leaf area [SLA], adult wood density, and seed mass). We used high-throughput DNA sequencing to identify fungal operational taxonomic units (OTUs) in the soil. Model predictions showed that seedlings of mid- and late-successional species had less leaf damage when the 12 most common AM fungi were abundant compared to when these fungi were absent. We also found that seedlings of mid-successional species were predicted to be more abundant when the 12 most common AM fungi were abundant compared to when these fungi were absent. In contrast, early-successional tree seedlings were predicted to be less abundant when the 12 most common AM fungi were abundant compared to when these fungi were absent. Finally, we showed that, among the 12 most common AM fungi, different AM fungi were correlated with functional trait characteristics of early- or late-successional species. Together, these results suggest that early-successional species might not rely as much as mid- and late-successional species on AM fungi, and AM fungi might accelerate forest succession.

A core-transient framework for trait-based community ecology: an example from a tropical tree seedling community.

Trait-based studies in community ecology have generally focused on the community as a unit where all species occur due to stochasticity, determinism or some mixture of the two. However, the processes governing population dynamics may vary greatly among species. We propose a core-transient framework for trait-based community studies where a core group of species has a strong link to the local environment while transient species have weaker responses to the environment. Consistent with the expectations of the framework, we found that common species exhibit clear linkages between performance and their environment and traits while rare species tend to have weaker or non-significant relationships. Ultimately, trait-based ecology should move beyond applying a set of processes to a community as a whole and towards quantifying inter-specific variation in the drivers of population dynamics that ultimately scale up to determine community structure.

Local neighbourhood and regional climatic contexts interact to explain tree performance.

Tree neighbourhood modelling has significantly contributed to our understanding of the mechanisms structuring communities. Investigations into the impact of neighbouring crowding on tree performance have generally been conducted at local scales, missing important regional-scale context such as the suitability of the climate for each species. Favourable climates may enhance tree performance, but this may come at the cost of increased neighbourhood crowding and competition negatively impacting survival and growth. Through the synthesis of continental-scale forest inventory and trait datasets from the northeast USA and Puerto Rico we present an analytical approach that elucidates the important interactions between local competitive and regional climatic contexts. Our results show strong asymmetries in competitive interactions and significant niche differences that are dependent on habitat suitability. The strong interaction between local neighbourhood and regional climate highlights the need for models that consider the interaction between these two processes that have been previously ignored.

Contrasting outcomes of species- and community-level analyses of the temporal consistency of functional composition.

Multiple anthropogenic drivers affect every natural community, and there is broad interest in using functional traits to understand and predict the consequences for future biodiversity. There is, however, no consensus regarding the choice of analytical methods. We contrast species- and community-level analyses of change in the functional composition for four traits related to drought tolerance using three decades of repeat censuses of trees in the 50-ha Forest Dynamics Plot on Barro Colorado Island, Panama. Community trait distributions shifted significantly through time, which may indicate a shift toward more drought tolerant species. However, at the species level, changes in abundance were unrelated to trait values. To reconcile these seemingly contrasting results, we evaluated species-specific contributions to the directional shifts observed at the community level. Abundance changes of just one to six of 312 species were responsible for the community-level shifts observed for each trait. Our results demonstrate that directional changes in community-level functional composition can result from idiosyncratic change in a few species rather than widespread community-wide changes associated with functional traits. Future analyses of directional change in natural communities should combine community-, species-, and possibly individual-level analyses to uncover relationships with function that can improve understanding and enable prediction.

Constancy in Functional Space across a Species Richness Anomaly.

The relationship between large-scale gradients in species richness and functional diversity provides important information regarding the mechanisms driving patterns of biodiversity. A classic hypothesis in ecology is that strong interspecific interactions should result in an increase in the functional volume of assemblages as the species richness increases, whereas climatic constraints may result in no change in functional volume. Most research of this kind examines latitudinal gradients in species richness, but the results are likely confounded by underlying gradients in climate and phylogenetic composition. We take an alternative approach that examines functional richness across a tree species richness anomaly where species richness doubles from Europe to eastern North America. The results demonstrate that the functional richness on both continents saturates at a similar point as species richness increases and that the packing of functional space becomes tighter. Further, the species richness anomaly is driven primarily by genera unique to North America, but those genera contribute less than expected functional richness to the region, indicating a high level of redundancy with genera shared between the continents. Taken together, the results indicate that the species richness anomaly is associated with diversification within a climatically constrained trait space. More generally, the work demonstrates the power of utilizing species richness anomalies in biodiversity research, particularly when they are coupled with information regarding organismal function.

Interspecific Functional Convergence and Divergence and Intraspecific Negative Density Dependence Underlie the Seed-to-Seedling Transition in Tropical Trees.

The seed-to-seedling transition constitutes a critical bottleneck in the life history of plants and represents a major determinant of species composition and abundance. However, we have surprisingly little knowledge regarding the forces driving this ontogenetic transition. Here we utilize information regarding organismal function to investigate the strength of intra- and interspecific negative density dependence during the seed-to-seedling transition in Puerto Rican tree species. Our analyses were implemented at individual sites and across an entire 16-ha forest plot, spanning 6 years. The functional richness of seedling assemblages was significantly lower than expected given the seed assemblages, but the functional evenness was significantly higher than expected, indicating the simultaneous importance of constraints on the overall phenotypic space and trait differences for successful transitions from seed to seedling. The results were consistent across years. Within species, we also found evidence for strong intraspecific negative density dependence, where the probability of transition was proportionally lower when in a site with high conspecific density. These results suggest that filtering of similar phenotypes across species and strong negative density dependence within and among species are simultaneously driving the structure and dynamics of tropical tree assemblages during this critical life-history transition.