Integrating tropical research into biology education is urgently needed.

Understanding tropical biology is important for solving complex problems such as climate change, biodiversity loss, and zoonotic pandemics, but biology curricula view research mostly via a temperate-zone lens. Integrating tropical research into biology education is urgently needed to tackle these issues.

Correction: Integrating tropical research into biology education is urgently needed.

[This corrects the article DOI: 10.1371/journal.pbio.3001674.].

Effects of lianas on forest biogeochemistry during their lives and afterlives.

Climate change and other anthropogenic disturbances are increasing liana abundance and biomass in many tropical and subtropical forests. While the effects of living lianas on species diversity, ecosystem carbon, and nutrient dynamics are receiving increasing attention, the role of dead lianas in forest ecosystems has been little studied and is poorly understood. Trees and lianas coexist as the major woody components of forests worldwide, but they have very different ecological strategies, with lianas relying on trees for mechanical support. Consequently, trees and lianas have evolved highly divergent stem, leaf, and root traits. Here we show that this trait divergence is likely to persist after death, into the afterlives of these organs, leading to divergent effects on forest biogeochemistry. We introduce a conceptual framework combining horizontal, vertical, and time dimensions for the effects of liana proliferation and liana tissue decomposition on ecosystem carbon and nutrient cycling. We propose a series of empirical studies comparing traits between lianas and trees to answer questions concerning the influence of trait afterlives on the decomposability of liana and tree organs. Such studies will increase our understanding of the contribution of lianas to terrestrial biogeochemical cycling, and help predict the effects of their increasing abundance.

Landscape-scale forest cover drives the predictability of forest regeneration across the Neotropics.

Abandonment of agricultural lands promotes the global expansion of secondary forests, which are critical for preserving biodiversity and ecosystem functions and services. Such roles largely depend, however, on two essential successional attributes, trajectory and recovery rate, which are expected to depend on landscape-scale forest cover in nonlinear ways. Using a multi-scale approach and a large vegetation dataset (843 plots, 3511 tree species) from 22 secondary forest chronosequences distributed across the Neotropics, we show that successional trajectories of woody plant species richness, stem density and basal area are less predictable in landscapes (4 km radius) with intermediate (40-60%) forest cover than in landscapes with high (greater than 60%) forest cover. This supports theory suggesting that high spatial and environmental heterogeneity in intermediately deforested landscapes can increase the variation of key ecological factors for forest recovery (e.g. seed dispersal and seedling recruitment), increasing the uncertainty of successional trajectories. Regarding the recovery rate, only species richness is positively related to forest cover in relatively small (1 km radius) landscapes. These findings highlight the importance of using a spatially explicit landscape approach in restoration initiatives and suggest that these initiatives can be more effective in more forested landscapes, especially if implemented across spatial extents of 1-4 km radius.

Phosphorus limitation of early growth differs between nitrogen-fixing and nonfixing dry tropical forest tree species.

Tropical forests are often characterized by low soil phosphorus (P) availability, suggesting that P limits plant performance. However, how seedlings from different functional types respond to soil P availability is poorly known but important for understanding and modeling forest dynamics under changing environmental conditions. We grew four nitrogen (N)-fixing Fabaceae and seven diverse non-N-fixing tropical dry forest tree species in a shade house under three P fertilization treatments and evaluated carbon (C) allocation responses, P demand, P-use, investment in P acquisition traits, and correlations among P acquisition traits. Nitrogen fixers grew larger with increasing P addition in contrast to non-N fixers, which showed fewer responses in C allocation and P use. Foliar P increased with P addition for both functional types, while P acquisition strategies did not vary among treatments but differed between functional types, with N fixers showing higher root phosphatase activity (RPA) than nonfixers. Growth responses suggest that N fixers are limited by P, but nonfixers may be limited by other resources. However, regardless of limitation, P acquisition traits such as mycorrhizal colonization and RPA were nonplastic across a steep P gradient. Differential limitation among plant functional types has implications for forest succession and earth system models.

Leaf habit affects the distribution of drought sensitivity but not water transport efficiency in the tropics.

Considering the global intensification of aridity in tropical biomes due to climate change, we need to understand what shapes the distribution of drought sensitivity in tropical plants. We conducted a pantropical data synthesis representing 1117 species to test whether xylem-specific hydraulic conductivity (KS ), water potential at leaf turgor loss (ΨTLP ) and water potential at 50% loss of KS (ΨP50 ) varied along climate gradients. The ΨTLP and ΨP50 increased with climatic moisture only for evergreen species, but KS did not. Species with high ΨTLP and ΨP50 values were associated with both dry and wet environments. However, drought-deciduous species showed high ΨTLP and ΨP50 values regardless of water availability, whereas evergreen species only in wet environments. All three traits showed a weak phylogenetic signal and a short half-life. These results suggest strong environmental controls on trait variance, which in turn is modulated by leaf habit along climatic moisture gradients in the tropics.

Demographic consequences of heterogeneity in conspecific density dependence among mast-fruiting tropical trees.

The role of conspecific density dependence (CDD) in the maintenance of species richness is a central focus of tropical forest ecology. However, tests of CDD often ignore the integrated effects of CDD over multiple life stages and their long-term impacts on population demography. We combined a 10-year time series of seed production, seedling recruitment and sapling and tree demography of three dominant Southeast Asian tree species that adopt a mast-fruiting phenology. We used these data to construct individual-based models that examine the effects of CDD on population growth rates (λ) across life-history stages. Recruitment was driven by positive CDD for all species, supporting the predator satiation hypothesis, while negative CDD affected seedling and sapling growth of two species, significantly reducing λ. This negative CDD on juvenile growth overshadowed the positive CDD of recruitment, suggesting the cumulative effects of CDD during seedling and sapling development has greater importance than the positive CDD during infrequent masting events. Overall, CDD varied among positive, neutral and negative effects across life-history stages for all species, suggesting that assessments of CDD on transitions between just two stages (e.g. seeds seedlings or juveniles mature trees) probably misrepresent the importance of CDD on population growth and stability.

Reduced ecosystem resilience quantifies fine-scale heterogeneity in tropical forest mortality responses to drought.

Sensitivity of forest mortality to drought in carbon-dense tropical forests remains fraught with uncertainty, while extreme droughts are predicted to be more frequent and intense. Here, the potential of temporal autocorrelation of high-frequency variability in Landsat Enhanced Vegetation Index (EVI), an indicator of ecosystem resilience, to predict spatial and temporal variations of forest biomass mortality is evaluated against in situ census observations for 64 site-year combinations in Costa Rican tropical dry forests during the 2015 ENSO drought. Temporal autocorrelation, within the optimal moving window of 24 months, demonstrated robust predictive power for in situ mortality (leave-one-out cross-validation R2  = 0.54), which allows for estimates of annual biomass mortality patterns at 30 m resolution. Subsequent spatial analysis showed substantial fine-scale heterogeneity of forest mortality patterns, largely driven by drought intensity and ecosystem properties related to plant water use such as forest deciduousness and topography. Highly deciduous forest patches demonstrated much lower mortality sensitivity to drought stress than less deciduous forest patches after elevation was controlled. Our results highlight the potential of high-resolution remote sensing to "fingerprint" forest mortality and the significant role of ecosystem heterogeneity in forest biomass resistance to drought.

Biomass resilience of Neotropical secondary forests.

Land-use change occurs nowhere more rapidly than in the tropics, where the imbalance between deforestation and forest regrowth has large consequences for the global carbon cycle. However, considerable uncertainty remains about the rate of biomass recovery in secondary forests, and how these rates are influenced by climate, landscape, and prior land use. Here we analyse aboveground biomass recovery during secondary succession in 45 forest sites and about 1,500 forest plots covering the major environmental gradients in the Neotropics. The studied secondary forests are highly productive and resilient. Aboveground biomass recovery after 20 years was on average 122 megagrams per hectare (Mg ha(-1)), corresponding to a net carbon uptake of 3.05 Mg C ha(-1) yr(-1), 11 times the uptake rate of old-growth forests. Aboveground biomass stocks took a median time of 66 years to recover to 90% of old-growth values. Aboveground biomass recovery after 20 years varied 11.3-fold (from 20 to 225 Mg ha(-1)) across sites, and this recovery increased with water availability (higher local rainfall and lower climatic water deficit). We present a biomass recovery map of Latin America, which illustrates geographical and climatic variation in carbon sequestration potential during forest regrowth. The map will support policies to minimize forest loss in areas where biomass resilience is naturally low (such as seasonally dry forest regions) and promote forest regeneration and restoration in humid tropical lowland areas with high biomass resilience.

Beyond leaf habit: generalities in plant function across 97 tropical dry forest tree species.

Leaf habit has been hypothesized to define a linkage between the slow-fast plant economic spectrum and the drought resistance-avoidance trade-off in tropical forests ('slow-safe vs fast-risky'). However, variation in hydraulic traits as a function of leaf habit has rarely been explored for a large number of species. We sampled leaf and branch functional traits of 97 tropical dry forest tree species from four sites to investigate whether patterns of trait variation varied consistently in relation to leaf habit along the 'slow-safe vs fast-risky' trade-off. Leaf habit explained from 0% to 43.69% of individual trait variation. We found that evergreen and semi-deciduous species differed in their location along the multivariate trait ordination when compared to deciduous species. While deciduous species showed consistent trait values, evergreen species trait values varied as a function of the site. Last, trait values varied in relation to the proportion of deciduous species in the plant community. We found that leaf habit describes the strategies that define drought avoidance and plant economics in tropical trees. However, leaf habit alone does not explain patterns of trait variation, which suggests quantifying site-specific or species-specific uncertainty in trait variation as the way forward.

Allometric scaling laws linking biomass and rooting depth vary across ontogeny and functional groups in tropical dry forest lianas and trees.

There are two theories about how allocation of metabolic products occurs. The allometric biomass partitioning theory (APT) suggests that all plants follow common allometric scaling rules. The optimal partitioning theory (OPT) predicts that plants allocate more biomass to the organ capturing the most limiting resource. Whole-plant harvests of mature and juvenile tropical deciduous trees, evergreen trees, and lianas and model simulations were used to address the following knowledge gaps: (1) Do mature lianas comply with the APT scaling laws or do they invest less biomass in stems compared to trees? (2) Do juveniles follow the same allocation patterns as mature individuals? (3) Is either leaf phenology or life form a predictor of rooting depth? It was found that: (1) mature lianas followed the same allometric scaling laws as trees; (2) juveniles and mature individuals do not follow the same allocation patterns; and (3) mature lianas had shallowest coarse roots and evergreen trees had the deepest. It was demonstrated that: (1) mature lianas invested proportionally similar biomass to stems as trees and not less, as expected; (2) lianas were not deeper-rooted than trees as had been previously proposed; and (3) evergreen trees had the deepest roots, which is necessary to maintain canopy during simulated dry seasons.

A catastrophic tropical drought kills hydraulically vulnerable tree species.

Drought-related tree mortality is now a widespread phenomenon predicted to increase in magnitude with climate change. However, the patterns of which species and trees are most vulnerable to drought, and the underlying mechanisms have remained elusive, in part due to the lack of relevant data and difficulty of predicting the location of catastrophic drought years in advance. We used long-term demographic records and extensive databases of functional traits and distribution patterns to understand the responses of 20-53 species to an extreme drought in a seasonally dry tropical forest in Costa Rica, which occurred during the 2015 El Niño Southern Oscillation event. Overall, species-specific mortality rates during the drought ranged from 0% to 34%, and varied little as a function of tree size. By contrast, hydraulic safety margins correlated well with probability of mortality among species, while morphological or leaf economics spectrum traits did not. This firmly suggests hydraulic traits as targets for future research.

Using large-scale tropical dry forest restoration to test successional theory.

Microclimatic conditions change dramatically as forests age and impose strong filters on community assembly during succession. Light availability is the most limiting environmental factor in tropical wet forest succession; by contrast, water availability is predicted to strongly influence tropical dry forest (TDF) successional dynamics. While mechanisms underlying TDF successional trajectories are not well understood, observational studies have demonstrated that TDF communities transition from being dominated by species with conservative traits to species with acquisitive traits, the opposite of tropical wet forest. Determining how functional traits predict TDF tree species' responses to changing environmental conditions could elucidate mechanisms underlying tree performance during TDF succession. We implemented a 6-ha restoration experiment on a degraded Vertisol in Costa Rica to determine (1) how TDF tree species with different resource-use strategies performed along a successional gradient and (2) how ecophysiological functional traits correlated with tree performance in simulated successional stages. We used two management treatments to simulate distinct successional stages including: clearing all remnant vegetation (early-succession), or interplanting seedlings with no clearing (mid-succession). We crossed these two management treatments (cleared/interplanted) with two species mixes with different resource-use strategies (acquisitive/conservative) to examine their interaction. Overall seedling survival after 2 yr was low, 15.1-26.4% in the four resource-use-strategy × management-treatment combinations, and did not differ between the management treatments or resource-use-strategy groups. However, seedling growth rates were dramatically higher for all species in the cleared treatment (year 1, 69.1% higher; year 2, 143.3% higher) and defined resource-use strategies had some capacity to explain seedling performance. Overall, ecophysiological traits were better predictors of species' growth and survival than resource-use strategies defined by leaf and stem traits such as specific leaf area. Moreover, ecophysiological traits related to water use had a stronger influence on seedling performance in the cleared, early-successional treatment, indicating that the influence of microclimatic conditions on tree survival and growth shifts predictably during TDF succession. Our findings suggest that ecophysiological traits should be explicitly considered to understand shifts in TDF functional composition during succession and that using these traits to design species mixes could greatly improve TDF restoration outcomes.

Trait-based signatures of cloud base height in a tropical cloud forest.

PREMISE: Clouds have profound consequences for ecosystem structure and function. Yet, the direct monitoring of clouds and their effects on biota is challenging especially in remote and topographically complex tropical cloud forests. We argue that known relationships between climate and the taxonomic and functional composition of plant communities may provide a fingerprint of cloud base height, thus providing a rapid and cost-effective assessment in remote tropical cloud forests. METHODS: To detect cloud base height, we compared species turnover and functional trait values among herbaceous and woody plant communities in an ecosystem dominated by cloud formation. We measured soil and air temperature, soil nutrient concentrations, and extracellular enzyme activity. We hypothesized that woody and herbaceous plants would provide signatures of cloud base height, as evidenced by abrupt shifts in both taxonomic composition and plant function. RESULTS: We demonstrated abrupt changes in taxonomic composition and the community- weighted mean of a key functional trait, specific leaf area, across elevation for both woody and herbaceous species, consistent with our predictions. However, abrupt taxonomic and functional changes occurred 100 m higher in elevation for herbaceous plants compared to woody ones. Soil temperature abruptly decreased where herbaceous taxonomic and functional turnover was high. Other environmental variables including soil biogeochemistry did not explain the abrupt change observed for woody plant communities. CONCLUSIONS: We provide evidence that a trait-based approach can be used to estimate cloud base height. We outline how rises in cloud base height and differential environmental requirements between growth forms can be distinguished using this approach.

Observed variation in soil properties can drive large variation in modelled forest functioning and composition during tropical forest secondary succession.

Censuses of tropical forest plots reveal large variation in biomass and plant composition. This paper evaluates whether such variation can emerge solely from realistic variation in a set of commonly measured soil chemical and physical properties. Controlled simulations were performed using a mechanistic model that includes forest dynamics, microbe-mediated biogeochemistry, and competition for nitrogen and phosphorus. Observations from 18 forest inventory plots in Guanacaste, Costa Rica were used to determine realistic variation in soil properties. In simulations of secondary succession, the across-plot range in plant biomass reached 30% of the mean and was attributable primarily to nutrient limitation and secondarily to soil texture differences that affected water availability. The contributions of different plant functional types to total biomass varied widely across plots and depended on soil nutrient status. In Central America, soil-induced variation in plant biomass increased with mean annual precipitation because of changes in nutrient limitation. In Central America, large variation in plant biomass and ecosystem composition arises mechanistically from realistic variation in soil properties. The degree of biomass and compositional variation is climate sensitive. In general, model predictions can be improved through better representation of soil nutrient processes, including their spatial variation.

Resilience of seed production to a severe El Niño-induced drought across functional groups and dispersal types.

More frequent and severe El Niño Southern Oscillations (ENSO) are causing episodic periods of decreased rainfall. Although the effects of these ENSO-induced droughts on tree growth and mortality have been well studied, the impacts on other demographic rates such as reproduction are less well known. We use a four-year seed rain dataset encompassing the most severe ENSO-induced drought in more than 30 years to assess the resilience (i.e., resistance and recovery) of the seed composition and abundance of three forest types in a tropical dry forest. We found that forest types showed distinct differences in the timing, duration, and intensity of drought during the ENSO event, which likely mediated seed composition shifts and resilience. Drought-deciduous species were particularly sensitive to the drought with overall poor resilience of seed production, whereby seed abundance of this functional group failed to recover to predrought levels even two years after the drought. Liana and wind-dispersed species were able to maintain seed production both during and after drought, suggesting that ENSO events promote early successional species or species with a colonization strategy. Combined, these results suggest that ENSO-induced drought mediates the establishment of functional groups and dispersal types suited for early successional conditions with more open canopies and reduced competition among plants. The effects of the ENSO-induced drought on seed composition and abundance were still evident two years after the event suggesting the recovery of seed production requires multiple years that may lead to shifts in forest composition and structure in the long term, with potential consequences for higher trophic levels like frugivores.

Lianas reduce carbon accumulation and storage in tropical forests.

Tropical forests store vast quantities of carbon, account for one-third of the carbon fixed by photosynthesis, and are a major sink in the global carbon cycle. Recent evidence suggests that competition between lianas (woody vines) and trees may reduce forest-wide carbon uptake; however, estimates of the impact of lianas on carbon dynamics of tropical forests are crucially lacking. Here we used a large-scale liana removal experiment and found that, at 3 y after liana removal, lianas reduced net above-ground carbon uptake (growth and recruitment minus mortality) by ∼76% per year, mostly by reducing tree growth. The loss of carbon uptake due to liana-induced mortality was four times greater in the control plots in which lianas were present, but high variation among plots prevented a significant difference among the treatments. Lianas altered how aboveground carbon was stored. In forests where lianas were present, the partitioning of forest aboveground net primary production was dominated by leaves (53.2%, compared with 39.2% in liana-free forests) at the expense of woody stems (from 28.9%, compared with 43.9%), resulting in a more rapid return of fixed carbon to the atmosphere. After 3 y of experimental liana removal, our results clearly demonstrate large differences in carbon cycling between forests with and without lianas. Combined with the recently reported increases in liana abundance, these results indicate that lianas are an important and increasing agent of change in the carbon dynamics of tropical forests.

Effects of soil type and light on height growth, biomass partitioning, and nitrogen dynamics on 22 species of tropical dry forest tree seedlings: Comparisons between legumes and nonlegumes.

PREMISE OF THE STUDY: The seedling stage is particularly vulnerable to resource limitation, with potential consequences for community composition. We investigated how light and soil variation affected early growth, biomass partitioning, morphology, and physiology of 22 tree species common in tropical dry forest, including eight legumes. Our hypothesis was that legume seedlings are better at taking advantage of increased resource availability, which contributes to their successful regeneration in tropical dry forests. METHODS: We grew seedlings in a full-factorial design under two light levels in two soil types that differed in nutrient concentrations and soil moisture. We measured height biweekly and, at final harvest, biomass partitioning, internode segments, leaf carbon, nitrogen, δ13C, and δ15N. KEY RESULTS: Legumes initially grew taller and maintained that height advantage over time under all experimental conditions. Legumes also had the highest final total biomass and water-use efficiency in the high-light and high-resource soil. For nitrogen-fixing legumes, the amount of nitrogen derived from fixation was highest in the richer soil. Although seed mass tended to be larger in legumes, seed size alone did not account for all the differences between legumes and nonlegumes. Both belowground and aboveground resources were limiting to early seedling growth and function. CONCLUSIONS: Legumes may have a different regeneration niche, in that they germinate rapidly and grow taller than other species immediately after germination, maximizing their performance when light and belowground resources are readily available, and potentially permitting them to take advantage of high light, nutrient, and water availability at the beginning of the wet season.

Biogeochemistry and Geographical Ecology: Embracing All Twenty-Five Elements Required to Build Organisms.

Biogeochemistry is a key but relatively neglected part of the abiotic template that underlies ecology. The template has a geography, one that is increasingly being rearranged in this era of global change. Justus von Liebig's law of the minimum has played a useful role in focusing attention on biogeochemical regulation of populations, but given that ∼25+ elements are required to build organisms and that these organisms use and deplete nutrients in aggregates of communities and ecosystems, we make the case that it is time to move on. We review available models that suggest the many different mechanisms that give rise to multiple elements, or colimitation. We then review recent empirical data that show that rates of decomposition and primary productivity may be limited by multiple elements. In that light, given the tropics' high species diversity and generally more weathered soils, we predict that colimitation at community and ecosystem scales is more prevalent closer to the equator. We conclude with suggestions for how to move forward with experimental studies of colimitation.