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.

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.

Interactions between all pairs of neighboring trees in 16 forests worldwide reveal details of unique ecological processes in each forest, and provide windows into their evolutionary histories.

When Darwin visited the Galapagos archipelago, he observed that, in spite of the islands' physical similarity, members of species that had dispersed to them recently were beginning to diverge from each other. He postulated that these divergences must have resulted primarily from interactions with sets of other species that had also diverged across these otherwise similar islands. By extrapolation, if Darwin is correct, such complex interactions must be driving species divergences across all ecosystems. However, many current general ecological theories that predict observed distributions of species in ecosystems do not take the details of between-species interactions into account. Here we quantify, in sixteen forest diversity plots (FDPs) worldwide, highly significant negative density-dependent (NDD) components of both conspecific and heterospecific between-tree interactions that affect the trees' distributions, growth, recruitment, and mortality. These interactions decline smoothly in significance with increasing physical distance between trees. They also tend to decline in significance with increasing phylogenetic distance between the trees, but each FDP exhibits its own unique pattern of exceptions to this overall decline. Unique patterns of between-species interactions in ecosystems, of the general type that Darwin postulated, are likely to have contributed to the exceptions. We test the power of our null-model method by using a deliberately modified data set, and show that the method easily identifies the modifications. We examine how some of the exceptions, at the Wind River (USA) FDP, reveal new details of a known allelopathic effect of one of the Wind River gymnosperm species. Finally, we explore how similar analyses can be used to investigate details of many types of interactions in these complex ecosystems, and can provide clues to the evolution of these interactions.

Pervasive decreases in living vegetation carbon turnover time across forest climate zones.

Forests play a major role in the global carbon cycle. Previous studies on the capacity of forests to sequester atmospheric CO2 have mostly focused on carbon uptake, but the roles of carbon turnover time and its spatiotemporal changes remain poorly understood. Here, we used long-term inventory data (1955 to 2018) from 695 mature forest plots to quantify temporal trends in living vegetation carbon turnover time across tropical, temperate, and cold climate zones, and compared plot data to 8 Earth system models (ESMs). Long-term plots consistently showed decreases in living vegetation carbon turnover time, likely driven by increased tree mortality across all major climate zones. Changes in living vegetation carbon turnover time were negatively correlated with CO2 enrichment in both forest plot data and ESM simulations. However, plot-based correlations between living vegetation carbon turnover time and climate drivers such as precipitation and temperature diverged from those of ESM simulations. Our analyses suggest that forest carbon sinks are likely to be constrained by a decrease in living vegetation carbon turnover time, and accurate projections of forest carbon sink dynamics will require an improved representation of tree mortality processes and their sensitivity to climate in ESMs.

Local canopy disturbance as an explanation for long-term increases in liana abundance.

Canopy disturbance explains liana abundance and distribution within tropical forests and thus may also explain the widespread pattern of increasing liana abundance; however, this hypothesis remains untested. We used a 10-year study (2007-2017) of 117,100 rooted lianas in an old-growth Panamanian forest to test whether local canopy disturbance explains increasing liana abundance. We found that liana density increased 29.2% and basal area 12.5%. The vast majority of these increases were associated with clonal stem proliferation following canopy disturbance, particularly in liana-dense, low-canopy gaps, which had far greater liana increases than did undisturbed forest. Lianas may be ecological niche constructors, arresting tree regeneration in gaps and thus creating a high-light environment that favours sustained liana proliferation. Our findings demonstrate that liana abundance is increasing rapidly and their ability to proliferate via copious clonal stem production in canopy gaps explains much of their increase in this and possibly other tropical forests.

Density-dependent adult recruitment in a low-density tropical tree.

The Janzen-Connell hypothesis is a well-known explanation for why tropical forests have large numbers of tree species. A fundamental prediction of the hypothesis is that the probability of adult recruitment is less in regions of high conspecific adult density, a pattern mediated by density-dependent mortality in juvenile life stages. Although there is strong evidence in many tree species that seeds, seedlings, and saplings suffer conspecific density-dependent mortality, no study has shown that adult tree recruitment is negatively density dependent. Density-dependent adult recruitment is necessary for the Janzen-Connell mechanism to regulate tree populations. Here, we report density-dependent adult recruitment in the population of Handroanthus guayacan, a wind-dispersed Neotropical canopy tree species. We use data from high-resolution remote sensing to track individual trees with proven capacity to flower in a lowland moist forest landscape in Panama and analyze these data in a Bayesian framework similar to capture-recapture analysis. We independently quantify probabilities of adult tree recruitment and detection and show that adult recruitment is negatively density dependent. The annualized probability of adult recruitment was 3.03% ⋅ year-1 Despite the detection of negative density dependence in adult recruitment, it was insufficient to stabilize the adult population of H. guayacan, which increased significantly in size over the decade of observation.

Lightning is a major cause of large tree mortality in a lowland neotropical forest.

The mortality rates of large trees are critical to determining carbon stocks in tropical forests, but the mechanisms of tropical tree mortality remain poorly understood. Lightning strikes thousands of tropical trees every day, but is commonly assumed to be a minor agent of tree mortality in most tropical forests. We use the first systematic quantification of lightning-caused mortality to show that lightning is a major cause of death for the largest trees in an old-growth lowland forest in Panama. A novel lightning strike location system together with field surveys of strike sites revealed that, on average, each strike directly kills 3.5 trees (> 10 cm diameter) and damages 11.4 more. Given lightning frequency data from the Earth Networks Total Lightning Network and historical total tree mortality rates for this site, we conclude that lightning accounts for 40.5% of the mortality of large trees (> 60 cm diameter) in the short term and probably contributes to an additional 9.0% of large tree deaths over the long term. Any changes in cloud-to-ground lightning frequency due to climatic change will alter tree mortality rates; projected 25-50% increases in lightning frequency would increase large tree mortality rates in this forest by 9-18%. The results of this study indicate that lightning plays a critical and previously underestimated role in tropical forest dynamics and carbon cycling.

Testing for changes in biomass dynamics in large-scale forest datasets.

Tropical forest responses to climate and atmospheric change are critical to the future of the global carbon budget. Recent studies have reported increases in estimated above-ground biomass (EAGB) stocks, productivity, and mortality in old-growth tropical forests. These increases could reflect a shift in forest functioning due to global change and/or long-lasting recovery from past disturbance. We introduce a novel approach to disentangle the relative contributions of these mechanisms by decomposing changes in whole-plot biomass fluxes into contributions from changes in the distribution of gap-successional stages and changes in fluxes for a given stage. Using 30 years of forest dynamic data at Barro Colorado Island, Panama, we investigated temporal variation in EAGB fluxes as a function of initial EAGB (EAGBi ) in 10 × 10 m quadrats. Productivity and mortality fluxes both increased strongly with initial quadrat EAGB. The distribution of EAGB (and thus EAGBi ) across quadrats hardly varied over 30 years (and seven censuses). EAGB fluxes as a function of EAGBi varied largely and significantly among census intervals, with notably higher productivity in 1985-1990 associated with recovery from the 1982-1983 El Niño event. Variation in whole-plot fluxes among census intervals was explained overwhelmingly by variation in fluxes as a function of EAGBi , with essentially no contribution from changes in EAGBi distributions. The high observed temporal variation in productivity and mortality suggests that this forest is very sensitive to climate variability. There was no consistent long-term trend in productivity, mortality, or biomass in this forest over 30 years, although the temporal variability in productivity and mortality was so strong that it could well mask a substantial trend. Accurate prediction of future tropical forest carbon budgets will require accounting for disturbance-recovery dynamics and understanding temporal variability in productivity and mortality.

Direct and indirect effects of climate on richness drive the latitudinal diversity gradient in forest trees.

Climate is widely recognised as an important determinant of the latitudinal diversity gradient. However, most existing studies make no distinction between direct and indirect effects of climate, which substantially hinders our understanding of how climate constrains biodiversity globally. Using data from 35 large forest plots, we test hypothesised relationships amongst climate, topography, forest structural attributes (stem abundance, tree size variation and stand basal area) and tree species richness to better understand drivers of latitudinal tree diversity patterns. Climate influences tree richness both directly, with more species in warm, moist, aseasonal climates and indirectly, with more species at higher stem abundance. These results imply direct limitation of species diversity by climatic stress and more rapid (co-)evolution and narrower niche partitioning in warm climates. They also support the idea that increased numbers of individuals associated with high primary productivity are partitioned to support a greater number of species.

Role of tree size in moist tropical forest carbon cycling and water deficit responses.

Drought disproportionately affects larger trees in tropical forests, but implications for forest composition and carbon (C) cycling in relation to dry season intensity remain poorly understood. In order to characterize how C cycling is shaped by tree size and drought adaptations and how these patterns relate to spatial and temporal variation in water deficit, we analyze data from three forest dynamics plots spanning a moisture gradient in Panama that have experienced El Niño droughts. At all sites, aboveground C cycle contributions peaked below 50-cm stem diameter, with stems ≥ 50 cm accounting for on average 59% of live aboveground biomass, 45% of woody productivity and 49% of woody mortality. The dominance of drought-avoidance strategies increased interactively with stem diameter and dry season intensity. Although size-related C cycle contributions did not vary systematically across the moisture gradient under nondrought conditions, woody mortality of larger trees was disproportionately elevated under El Niño drought stress. Thus, large (> 50 cm) stems, which strongly mediate but do not necessarily dominate C cycling, have drought adaptations that compensate for their more challenging hydraulic environment, particularly in drier climates. However, these adaptations do not fully buffer the effects of severe drought, and increased large tree mortality dominates ecosystem-level drought responses.

Variation in hydroclimate sustains tropical forest biomass and promotes functional diversity.

The fate of tropical forests under climate change is unclear as a result, in part, of the uncertainty in projected changes in precipitation and in the ability of vegetation models to capture the effects of drought-induced mortality on aboveground biomass (AGB). We evaluated the ability of a terrestrial biosphere model with demography and hydrodynamics (Ecosystem Demography, ED2-hydro) to simulate AGB and mortality of four tropical tree plant functional types (PFTs) that operate along light- and water-use axes. Model predictions were compared with observations of canopy trees at Barro Colorado Island (BCI), Panama. We then assessed the implications of eight hypothetical precipitation scenarios, including increased annual precipitation, reduced inter-annual variation, El Niño-related droughts and drier wet or dry seasons, on AGB and functional diversity of the model forest. When forced with observed meteorology, ED2-hydro predictions capture multiple BCI benchmarks. ED2-hydro predicts that AGB will be sustained under lower rainfall via shifts in the functional composition of the forest, except under the drier dry-season scenario. These results support the hypothesis that inter-annual variation in mean and seasonal precipitation promotes the coexistence of functionally diverse PFTs because of the relative differences in mortality rates. If the hydroclimate becomes chronically drier or wetter, functional evenness related to drought tolerance may decline.

Community-level species' correlated distribution can be scale-independent and related to the evenness of abundance.

The spatial distribution of species is not random; instead, individuals tend to gather, resulting in a non-random pattern. Previous studies used the independent negative binomial distribution (NBD) to model the distributional aggregation of a single species, in which the independence of the distribution of individuals of a species in different quadrats had been assumed. This way of analyzing aggregation will result in the scale-dependent estimation of the aggregation or shape parameter. However, because non-random (and therefore non-independent) distribution of individuals of a species in a finite area can be caused by either correlated or clumped distribution of individuals of a species between neighboring sites, an alternative model would assume that the distribution of individuals of a species over different sampling areas is multinomial. Here, we showed that, by assuming that regional species abundance followed a NBD while using a multinomial distribution to assign individuals of species in different non-overlapped sampling quadrats that are from a partition of the entire region (quantifying positive correlation or synchrony), the estimation of the shape parameter in this probabilistic model, which is the negative multinomial distribution (NMD), was scale-invariant (i.e., the estimated shape parameter is identical across different partitions of the study region). Accordingly, the estimation of the shape parameter was related to regional species distribution alone. This implied that, the shape parameter at the community level, using the NMD model, reflected the evenness of interspecific abundance. As a comparison, if the distribution of individuals of a single species followed independent NBDs as studied previously, the shape parameter would measure the evenness of intraspecific abundance (quantifying single-species' distributional aggregation). Moreover, our study highlighted the necessity for adjusting the model for the effects of unsampled species when studying community-level distributional patterns. Collectively, as long as a target area is partitioned into non-overlapping quadrats (no matter how their sizes vary), the proposed NMD model in this study, along with the independent NBDs model, can be jointly formulated as a framework to reconcile the scale-dependent debate on the shape parameter, unifying the relationship between inter- or intraspecific abundance and distributional patterns.

Effects of biotic interactions on tropical tree performance depend on abiotic conditions.

Predicting biotic responses to environmental change requires understanding the joint effects of abiotic conditions and biotic interactions on community dynamics. One major challenge is to separate the potentially confounding effects of abiotic environmental variation and local biotic interactions on individual performance. The stress gradient hypothesis (SGH) addresses this issue directly by predicting that the effects of biotic interactions on performance become more positive as the abiotic environment becomes more stressful. It is unclear, however, how the predictions of the SGH apply to plants of differing functional strategies in diverse communities. We asked (1) how the effect of crowding on performance (growth and survival) of trees varies across a precipitation gradient, and (2) how functional strategies (as measured by two key traits: wood density and leaf mass per area, LMA) mediate average demographic rates and responses to crowding across the gradient. We built trait-based neighborhood models of growth and survival across a regional precipitation gradient where increasing precipitation is associated with reduced abiotic stress. In total, our dataset comprised ~170,000 individual trees belonging to 252 species. The effect of crowding on tree performance varied across the gradient; crowding negatively affected growth across plots and positively affected survival in the wettest plot. Functional traits mediated average demographic rates across the gradient, but we did not find clear evidence that the strength of these responses depends on species' traits. Our study lends support to the SGH and demonstrates how a trait-based perspective can advance these concepts by linking the diversity of species interactions with functional variation across abiotic gradients.

Resolving the paradox of clumped seed dispersal: positive density and distance dependence in a bat-dispersed species.

One of the hypothesized benefits of seed dispersal is to escape density- and distance-responsive, host-specific, natural enemies near maternal plants where conspecific seed and seedling densities are high. Such high conspecific neighbor densities typically result in lower offspring growth and survival (i.e., negative density-dependent effects), yet many dispersal modes result in clumped seed distributions. New World leaf-nosed bats transport fruits to their feeding roosts and deposit seeds, thereby creating high-density seed/seedling patches beneath feeding roosts in heterospecific trees away from maternal trees, which seemingly nullifies a key benefit of seed dispersal. Such dispersal may still be adaptive if negative density-dependent effects are reduced under feeding roosts or if the benefit of being dispersed away from maternal trees outweighs negative effects of conspecific seed/seedling density below roosts. We mapped the entire post-germination population of a bat-dispersed tree species Calophyllum longifolium (Calophyllaceae) in a 50-ha plot on Barro Colorado Island, Panama in each of three successive years. We tested two hypotheses: (1) distance-dependent effects are stronger than density-dependent effects on seedling performance because seedlings far from conspecific adults are more likely to escape natural enemies even when at high densities and (2) negative density-dependent effects will be reduced far from vs. near conspecific adults. Density and distance were naturally decoupled, as expected. However, in contrast to our expectation, we found positive density effects on seedling survival and density-dependent effects did not differ with distance from conspecific adults. Both density and distance had positive effects on seedling survival when considered together, while only year had a significant effect on seedling growth. Thus, both being dispersed under bat feeding roosts and escaping the vicinity of conspecific adults were beneficial for C. longifolium seedling survival, supporting the directed dispersal and escape hypotheses, respectively. Despite resulting in high densities of conspecific seedlings, favorable habitat under bat feeding roosts and lack of negative density-dependent effects appear to provide evolutionary advantages in C. longifolium.

Surviving in a Cosexual World: A Cost-Benefit Analysis of Dioecy in Tropical Trees.

Dioecy has a demographic disadvantage compared with hermaphroditism: only about half of reproductive adults produce seeds. Dioecious species must therefore have fitness advantages to compensate for this cost through increased survival, growth, and/or reproduction. We used a full life cycle approach to quantify the demographic costs and benefits associated with dioecy while controlling for demographic differences between dioecious and hermaphroditic species related to other functional traits. The advantage of this novel approach is that we can focus on the effect of breeding system across a diverse tree community. We built a composite integral projection model for hermaphroditic and dioecious tree populations from Barro Colorado Island, Panama, using long-term demographic and newly collected reproductive data. Integration of all costs and benefits showed that compensation was realized through increased seed production, resulting in no net costs of dioecy. Compensation was also facilitated by the low contribution of reproduction to population growth. Estimated positive effects of dioecy on tree growth and survival were small and insignificant for population growth rates. Our model revealed that, for long-lived organisms, the cost of having males is smaller than generally expected. Hence, little compensation is required for dioecious species to maintain population growth rates similar to those of hermaphroditic species.

Abiotic niche partitioning and negative density dependence drive tree seedling survival in a tropical forest.

In tropical tree communities, processes occurring during early life stages play a critical role in shaping forest composition and diversity through differences in species' performance. Predicting the future of tropical forests depends on a solid understanding of the drivers of seedling survival. At the same time, factors determining spatial and temporal patterns of seedling survival can play a large role in permitting species coexistence in diverse communities. Using long-term data on the survival of more than 45 000 seedlings of 238 species in a Neotropical forest, we assessed the relative importance of key abiotic and biotic neighbourhood variables thought to influence individual seedling survival and tested whether species vary significantly in their responses to these variables, consistent with niche differences. At the community level, seedling survival was significantly correlated with plant size, topographic habitat, neighbourhood densities of conspecific seedlings, conspecific and heterospecific trees and annual variation in water availability, in descending order of effect size. Additionally, we found significant variation among species in their sensitivity to light and water availability, as well as in their survival within different topographic habitats, indicating the potential for niche differentiation among species that could allow for species coexistence.

Adult mortality in a low-density tree population using high-resolution remote sensing.

We developed a statistical framework to quantify mortality rates in canopy trees observed using time series from high-resolution remote sensing. By timing the acquisition of remote sensing data with synchronous annual flowering in the canopy tree species Handroanthus guayacan, we made 2,596 unique detections of 1,006 individual adult trees within 18,883 observation attempts on Barro Colorado Island, Panama (BCI) during an 11-yr period. There were 1,057 observation attempts that resulted in missing data due to cloud cover or incomplete spatial coverage. Using the fraction of 123 individuals from an independent field sample that were detected by satellite data (109 individuals, 88.6%), we estimate that the adult population for this species on BCI was 1,135 individuals. We used a Bayesian state-space model that explicitly accounted for the probability of tree detection and missing observations to compute an annual adult mortality rate of 0.2%·yr-1 (SE = 0.1, 95% CI = 0.06-0.45). An independent estimate of the adult mortality rate from 260 field-checked trees closely matched the landscape-scale estimate (0.33%·yr-1 , SE = 0.16, 95% CI = 0.12-0.74). Our proof-of-concept study shows that one can remotely estimate adult mortality rates for canopy tree species precisely in the presence of variable detection and missing observations.

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.

The use of soil pollen to determine the sex of overhead individuals of a temperate dioecious shrub.

PREMISE OF THE STUDY: In dioecious species, determining the sex of individual plants from one-time phenological observations is rarely feasible when some individuals capable of reproducing are not flowering or fruiting at the time of observation. Currently, sexing those individuals requires long-term phenological data on individuals and populations, but such data are rarely available or feasible to collect. We tested the hypothesis that differences in soil pollen concentrations beneath the crowns of female and male plants would exist and be sufficient to reliably determine the sex of the individual plant overhead in a dioecious species. We predicted that soil pollen concentrations beneath male plants would be significantly higher than beneath female plants because only males produce pollen and pollen should accumulate in the soil underneath the male plants over repeated flowering events. METHODS: We collected samples from surface soil under both sexes of the insect-pollinated dioecious shrub, Aucuba japonica (Garryaceae). KEY RESULTS: Pollen grains were present in surface soil in both Oe and A horizons, and mean pollen concentration under males was significantly higher than under females. Pollen concentrations beneath males were positively correlated with male plant height, potentially reflecting greater pollen production by larger individuals. CONCLUSIONS: Considering the small plant size and relatively low pollen production of A. japonica, this method may hold promise for sexing other dioecious species in the absence of direct phenological data. Our phenology-free and relatively low-cost method for sexing dioecious plants may be especially useful in tropical forests where many species are dioecious.