ZooTraits: An R shiny app for exploring animal trait data for ecological and evolutionary research.

Animal trait data are scattered across several datasets, making it challenging to compile and compare trait information across different groups. For plants, the TRY database has been an unwavering success for those ecologists interested in addressing how plant traits influence a wide variety of processes and patterns, but the same is not true for most animal taxonomic groups. Here, we introduce ZooTraits, a Shiny app designed to help users explore and obtain animal trait data for research in ecology and evolution. ZooTraits was developed to tackle the challenge of finding in a single site information of multiple trait datasets and facilitating access to traits by providing an easy-to-use, open-source platform. This app combines datasets centralized in the Open Trait Network, raw data from the AnimalTraits database, and trait information for animals compiled by Gonçalves-Souza et al. (2023, Ecology and Evolution 13, e10016). Importantly, the ZooTraits app can be accessed freely and provides a user-friendly interface through three functionalities that will allow users to easily visualize, compare, download, and upload trait data across the animal tree of life-ExploreTrait, FeedTrait, and GetTrait. By using ExploreTrait and GetTrait, users can explore, compare, and extract 3954 trait records from 23,394 species centralized in the Open Traits Network, and trait data for ~2000 species from the AnimalTraits database. The app summarizes trait information for numerous taxonomic groups within the Animal Kingdom, encompassing data from diverse aquatic and terrestrial ecosystems and various geographic regions worldwide. Moreover, ZooTraits enables researchers to upload trait information, serving as a hub for a continually expanding global trait database. By promoting the centralization of trait datasets and offering a platform for data sharing, ZooTraits is facilitating advancements in trait-based ecological and evolutionary studies. We hope that other trait databases will evolve to mirror the approach we have outlined here.

Upscaling the effect of traits in response to drought: The relative importance of safety-efficiency and acquisitive-conservation functional axes.

We tested the idea that functional trade-offs that underlie species tolerance to drought-driven shifts in community composition via their effects on demographic processes and subsequently on shifts in species' abundance. Using data from 298 tree species from tropical dry forests during the extreme ENSO-2015, we scaled-up the effects of trait trade-offs from individuals to communities. Conservative wood and leaf traits favoured slow tree growth, increased tree survival and positively impacted species abundance and dominance at the community-level. Safe hydraulic traits, on the other hand, were related to demography but did not affect species abundance and communities. The persistent effects of the conservative-acquisitive trade-off across organizational levels is promising for generalization and predictability of tree communities. However, the safety-efficient trade-off showed more intricate effects on performance. Our results demonstrated the complex pathways in which traits scale up to communities, highlighting the importance of considering a wide range of traits and performance processes.

More than 10,000 pre-Columbian earthworks are still hidden throughout Amazonia.

Indigenous societies are known to have occupied the Amazon basin for more than 12,000 years, but the scale of their influence on Amazonian forests remains uncertain. We report the discovery, using LIDAR (light detection and ranging) information from across the basin, of 24 previously undetected pre-Columbian earthworks beneath the forest canopy. Modeled distribution and abundance of large-scale archaeological sites across Amazonia suggest that between 10,272 and 23,648 sites remain to be discovered and that most will be found in the southwest. We also identified 53 domesticated tree species significantly associated with earthwork occurrence probability, likely suggesting past management practices. Closed-canopy forests across Amazonia are likely to contain thousands of undiscovered archaeological sites around which pre-Columbian societies actively modified forests, a discovery that opens opportunities for better understanding the magnitude of ancient human influence on Amazonia and its current state.

The interplay of drought and hurricanes on tree recovery: insights from dynamic and weak functional responses.

Identifying the functional traits that enable recovery after extreme events is necessary for assessing forest persistence and functioning. However, the variability of traits mediating responses to disturbances presents a significant limitation, as these relationships may be contingent on the type of disturbance and change over time. This study investigates the effects of traits on tree growth-for short and longer terms-in response to two vastly different extreme climatic events (droughts and hurricanes) in a Puerto Rican forest. I found that trees display a dynamic functional response to extreme climatic events. Leaf traits associated with efficient photosynthesis mediated faster tree growth after hurricanes, while trees with low wood density and high water use efficiency displayed faster growth after drought. In the longer term, over both drought and hurricanes, tree size was the only significant predictor of growth, with faster growth for smaller trees. However, despite finding significant trait-growth relationships, the predictive power of traits was overall low. As the frequency of extreme events increases due to climate change, understanding the dynamic relationships between traits and tree growth is necessary for identifying strategies for recovery.

Characterizing tree trait variance over spatiotemporal scales.

Beyond the study of the mean, functional ecology lacks a concise characterization of trait variance patterns across spatiotemporal scales. Traits are measured in different ways, using different metrics, and at different spatial (and rarely temporal) scales. This study expands on previous research by applying a ubiquitous and widely used empirical model-Taylor's Power Law-to functional trait variance with the goal of identifying general patterns of trait variance scaling (the behavior of trait variance across scales). We compiled data on tree seedling communities monitored over 10 years across 213 2 m2 plots and functional trait data from a subtropical forest in Puerto Rico. We examined trait-based Taylor's Power Law at nested spatial and temporal scales. The scaling of variance with the mean was idiosyncratic across traits suggesting that the drivers of variation are likely to differ across traits that may make variance scaling theory elusive. However, slopes varied more in space than through time, suggesting that spatial environmental variability may have a larger role in driving trait variance than temporal variability. Empirical models that characterize taxonomic patterns across spatiotemporal scales, like Taylor's Power Law, can provide an insight into the scaling of functional traits, a necessary next step toward a more predictive trait-based ecology.

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.

Tree mycorrhizal type mediates conspecific negative density dependence effects on seedling herbivory, growth, and survival.

Tree mycorrhizal type plays an important role in promoting plant species diversity and coexistence, via its mediating role in conspecific negative density dependence (CNDD), i.e., the process by which an individual's performance is impaired by the density of conspecific plants. Previous findings suggest that ectomycorrhizal (EM) tree species are generally less susceptible to CNDD than arbuscular mycorrhizal (AM) tree species, due to the chemical and physical protection that EM fungi provide their host with. We examined how CNDD effects on leaf herbivory, seedling growth, and survival differ between AM and EM seedlings of ten tree species collected over 3 years in an old-growth temperate forest in northeastern China. We found that AM and EM seedlings differed in how conspecific density affected their leaf herbivory, seedling growth, and survival. Specifically, AM seedlings leaf herbivory rates significantly increased with increasing conspecific seedling and adult density, and their growth and survival rates decreased with increasing conspecific adult density, these patterns were, however, absent in EM seedlings. Our work suggests that AM seedlings have a performance disadvantage relative to EM seedlings related to the negative effects from conspecific neighbors. We highlight the importance of integrating information on seedling leaf herbivory, seedling growth, to provide further understanding on potential mechanisms driving differences in CNDD between AM and EM tree seedlings.

Perceptions by early career tropical researchers on the impact of COVID-19 six months into the pandemic.

The impacts of COVID-19 on early career tropical researchers are diverse and complex, including lack of funding opportunities, limitations to conducting fieldwork in remote places, reduced collaborations and networking, and difficulties when living and collecting data abroad. Here, we examine the current and future impacts of the COVID-19 pandemic on this population through a survey of 213 students and early career tropical researchers from around the world. As of September 2020, 55% of participants had already experienced financial repercussions due to the pandemic. Future worries were diverse and included equal concern regarding advancement (collaborations and networking), job uncertainty, fieldwork, and funding, as well as mental health concerns. Successful strategies to support student and early career researchers with regards to the pandemic should include mentoring from those in more advanced career positions on how to reframe research that is no longer feasible to complete as originally intended. Additionally, those responsible for hiring decisions should not penalize applicants for gaps in productivity during this time.

Los impactos de COVID­19 en investigadores tropicales en etapas tempranas de su carrera son diversos y complejos incluyendo la falta de oportunidades de financiamiento, limitaciones para realizar trabajo de campo en lugares remotos, la reducción en las posibilidades de establecer nuevas colaboraciones, y dificultades para vivir y colectar datos en el extranjero. En este estudio examinamos los impactos actuales y futuros de la pandemia COVID­19 en este grupo por medio de una encuesta a 213 estudiantes e investigadores tropicales que están en etapas tempranas de su carrera de todo el mundo. A septiembre de 2020, el 55% de los participantes ya habían experimentado repercusiones financiaras debido a la pandemia. Las preocupaciones sobre el futuro fueron diversas incluyendo una inquietud general con respecto al avance de las colaboraciones, la incertidumbre laboral, el trabajo de campo, la posibilidad de obtener financiación y la salud mental. Sugerimos que estrategias exitosas para apoyar estudiantes e investigadores en etapas tempranas de su carrera en tiempos de pandemia deben incluir la tutoría de aquellos en posiciones profesionales más avanzadas que apoyen y guíen en el proceso de re­plantear proyectos de investigación que ya no sean factibles. Además, a aquellos responsables de las decisiones de contratación deben ser flexibles y entender las posibles brechas en productividad durante este periodo.

Relating leaf traits to seedling performance in a tropical forest: building a hierarchical functional framework.

Trait-based approaches have been extensively used in community ecology to provide a mechanistic understanding of the drivers of community assembly. However, a foundational assumption of the trait framework, traits relate to performance, has been mainly examined through univariate relationships that simplify the complex phenotypic integration of organisms. We evaluate a conceptual framework in which traits are organized hierarchically combining trait information at the individual- and species-level from biomass allocation and organ-level traits. We focus on photosynthetic traits and predict that the positive effects of increasing plant leaf mass on growth depend on species-level leaf traits. We modeled growth data on more than 1,500 seedlings from 97 seedling species from a tropical forest in China. We found that seedling growth increases with allocation to leaves (high leaf area ratio and leaf mass fraction) and this effect is accentuated for species with high specific leaf area and leaf area. Also, we found that light has a significant effect on growth, and this effect is additive with leaf allocation traits. Our work offers an approach to gain further understanding of the effects of traits on the whole plant-level growth via a hierarchical framework including organ-level and biomass allocation traits at species and individual levels.

Tree seedling trait optimization and growth in response to local-scale soil and light variability.

At local scales, it has been suggested that high levels of resources lead to increased tree growth via trait optimization (highly peaked trait distribution). However, this contrasts with (1) theories that suggest that trait optimization and high growth occur in the most common resource level and (2) empirical evidence showing that high trait optimization can be also found at low resource levels. This raises the question of how are traits and growth optimized in highly diverse plant communities. Here, we propose a series of hypotheses about how traits and growth are expected to be maximized under different resource levels (low, the most common, and high) in tree seedling communities from a subtropical forest in Puerto Rico, USA. We studied the variation in the distribution of biomass allocation and leaf traits and seedlings growth rate along four resource gradients: light availability (canopy openness) and soil K, Mg, and N content. Our analyses consisted of comparing trait kurtosis (a measurement of trait optimization), community trait means, and relative growth rates at three resource levels (low, common, and high). Trait optimization varied across the three resource levels depending on the type of resource and trait, with leaf traits being optimized under high N and in the most common K and Mg conditions, but not at any of the light levels. Also, seedling growth increased at high-light conditions and high N and K but was not related to trait kurtosis. Our results indicate that local-scale variability of soil fertility and understory light conditions result in shifts in species ecological strategies that increase growth despite a weak trait optimization, suggesting the existence of alternative phenotypes that achieve similar high performance. Uncovering the links between abiotic factors, functional trait diversity and performance is necessary to better predict tree responses to future changes in abiotic conditions.

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.

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.

Climate sensitive size-dependent survival in tropical trees.

Survival rates of large trees determine forest biomass dynamics. Survival rates of small trees have been linked to mechanisms that maintain biodiversity across tropical forests. How species survival rates change with size offers insight into the links between biodiversity and ecosystem function across tropical forests. We tested patterns of size-dependent tree survival across the tropics using data from 1,781 species and over 2 million individuals to assess whether tropical forests can be characterized by size-dependent life-history survival strategies. We found that species were classifiable into four 'survival modes' that explain life-history variation that shapes carbon cycling and the relative abundance within forests. Frequently collected functional traits, such as wood density, leaf mass per area and seed mass, were not generally predictive of the survival modes of species. Mean annual temperature and cumulative water deficit predicted the proportion of biomass of survival modes, indicating important links between evolutionary strategies, climate and carbon cycling. The application of survival modes in demographic simulations predicted biomass change across forest sites. Our results reveal globally identifiable size-dependent survival strategies that differ across diverse systems in a consistent way. The abundance of survival modes and interaction with climate ultimately determine forest structure, carbon storage in biomass and future forest trajectories.

Abundance-dependent effects of neighbourhood dissimilarity and growth rank reversal in a neotropical forest.

Why tropical forests harbour an exceptional number of species with striking differences in abundances remains an open question. We propose a theoretical framework to address this question in which rare species may have different extirpation risks depending on species ranks in tree growth and sensitivities to neighbourhood interactions. To evaluate the framework, we studied tree growth and its responses to neighbourhood dissimilarity (ND) in traits and phylogeny for 146 species in a neotropical forest. We found that tree growth was positively related to ND, and common species were more strongly affected by ND than rare species, which may help delay dominance of common species. Rare species grew more slowly at the community-wide average ND than common species. But rare species grew faster when common species tended to dominate locally, which may help reduce extirpation risk of rare species. Our study highlights that tree growth rank among species depends on their responses to neighbourhood interactions, which can be important in fostering diversity maintenance in tropical forests.

Tree co-occurrence and transcriptomic response to drought.

The distribution and co-occurrence of species are partly the outcome of their interactions with environmental drivers. Drought is a key driver related to the distribution of plant species. Drought events continue to increase in frequency and severity and identifying those aspects of plant function that are related to drought is critical. Here, we perform a community-level analysis of gene expression in relation to experimental drought and relate the similarity in gene set enrichment across species to their natural co-occurrence. Species with similar gene set enrichment in response to experimental drought tend to non-randomly co-occur in a natural stand. We demonstrate that similarity in the transcriptomic response of species to drought is a significantly better indicator of natural co-occurrence than measures of functional trait similarity and phylogenetic relatedness and that transcriptomics has the capacity to greatly enhance ecological investigations of species distributions and community structure.

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.

Linking individual-level functional traits to tree growth in a subtropical forest.

Forging strong links between traits and performance is essential for understanding and predicting community assembly and dynamics. Functional trait analyses of trees that have correlated single-trait values with measures of performance such as growth and mortality have generally found weak relationships. A reason for these weak relationships is the failure to use individual-level trait data while simultaneously putting that data into the context of the abiotic setting, neighborhood composition, and the remaining axes constituting the overall phenotype. Here, utilizing detailed growth and trait data for 59 species of trees in a subtropical forest, we demonstrate that the individual-level functional trait values are strongly related to individual growth rates, and that the strength of these relationships critically depends on the context of that individual. We argue that our understanding of trait-performance relationships can be greatly improved with individual-level data so long as that data is put into the proper context.

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.

Commonness, rarity, and intraspecific variation in traits and performance in tropical tree seedlings.

One of the few rules in ecology is that communities are composed of many rare and few common species. Trait-based investigations of abundance distributions have generally focused on species-mean trait values with mixed success. Here, using large tropical tree seedling datasets in China and Puerto Rico, we take an alternative approach that considers the magnitude of intraspecific variation in traits and growth as it relates to species abundance. We find that common species are less variable in their traits and growth. Common species also occupy core positions within community trait space indicating that they are finely tuned for the available conditions. Rare species are functionally peripheral and are likely transients struggling for success in the given environment. The work highlights the importance of considering intraspecific variation in trait-based ecology and demonstrates asymmetry in the magnitude of intraspecific variation among species is critical for understanding of how traits are related to abundance.