Tree demographic strategies largely overlap across succession in Neotropical wet and dry forest communities.

Secondary tropical forests play an increasingly important role in carbon budgets and biodiversity conservation. Understanding successional trajectories is therefore imperative for guiding forest restoration and climate change mitigation efforts. Forest succession is driven by the demographic strategies-combinations of growth, mortality and recruitment rates-of the tree species in the community. However, our understanding of demographic diversity in tropical tree species stems almost exclusively from old-growth forests. Here, we assembled demographic information from repeated forest inventories along chronosequences in two wet (Costa Rica, Panama) and two dry (Mexico) Neotropical forests to assess whether the ranges of demographic strategies present in a community shift across succession. We calculated demographic rates for >500 tree species while controlling for canopy status to compare demographic diversity (i.e., the ranges of demographic strategies) in early successional (0-30 years), late successional (30-120 years) and old-growth forests using two-dimensional hypervolumes of pairs of demographic rates. Ranges of demographic strategies largely overlapped across successional stages, and early successional stages already covered the full spectrum of demographic strategies found in old-growth forests. An exception was a group of species characterized by exceptionally high mortality rates that was confined to early successional stages in the two wet forests. The range of demographic strategies did not expand with succession. Our results suggest that studies of long-term forest monitoring plots in old-growth forests, from which most of our current understanding of demographic strategies of tropical tree species is derived, are surprisingly representative of demographic diversity in general, but do not replace the need for further studies in secondary forests.

Successional theories.

Succession is a fundamental concept in ecology because it indicates how species populations, communities, and ecosystems change over time on new substrate or after a disturbance. A mechanistic understanding of succession is needed to predict how ecosystems will respond to land-use change and to design effective ecosystem restoration strategies. Yet, despite a century of conceptual advances a comprehensive successional theory is lacking. Here we provide an overview of 19 successional theories ('models') and their key points, group them based on conceptual similarity, explain conceptual development in successional ideas and provide suggestions how to move forward. Four groups of models can be recognised. The first group (patch & plants) focuses on plants at the patch level and consists of three subgroups that originated in the early 20th century. One subgroup focuses on the processes (dispersal, establishment, and performance) that operate sequentially during succession. Another subgroup emphasises individualistic species responses during succession, and how this is driven by species traits. A last subgroup focuses on how vegetation structure and underlying demographic processes change during succession. A second group of models (ecosystems) provides a more holistic view of succession by considering the ecosystem, its biota, interactions, diversity, and ecosystem structure and processes. The third group (landscape) considers a larger spatial scale and includes the effect of the surrounding landscape matrix on succession as the distance to neighbouring vegetation patches determines the potential for seed dispersal, and the quality of the neighbouring patches determines the abundance and composition of seed sources and biotic dispersal vectors. A fourth group (socio-ecological systems) includes the human component by focusing on socio-ecological systems where management practices have long-lasting legacies on successional pathways and where regrowing vegetations deliver a range of ecosystem services to local and global stakeholders. The four groups of models differ in spatial scale (patch, landscape) or organisational level (plant species, ecosystem, socio-ecological system), increase in scale and scope, and reflect the increasingly broader perspective on succession over time. They coincide approximately with four periods that reflect the prevailing view of succession of that time, although all views still coexist. The four successional views are: succession of plants (from 1910 onwards) where succession was seen through the lens of species replacement; succession of communities and ecosystems (from 1965 onwards) when there was a more holistic view of succession; succession in landscapes (from 2000 onwards) when it was realised that the structure and composition of landscapes strongly impact successional pathways, and increased remote-sensing technology allowed for a better quantification of the landscape context; and succession with people (from 2015 onwards) when it was realised that people and societal drivers have strong effects on successional pathways, that ecosystem processes and services are important for human well-being, and that restoration is most successful when it is done by and for local people. Our review suggests that the hierarchical successional framework of Pickett is the best starting point to move forward as this framework already includes several factors, and because it is flexible, enabling application to different systems. The framework focuses mainly on species replacement and could be improved by focusing on succession occurring at different hierarchical scales (population, community, ecosystem, socio-ecological system), and by integrating it with more recent developments and other successional models: by considering different spatial scales (landscape, region), temporal scales (ecosystem processes occurring over centuries, and evolution), and by taking the effects of the surrounding landscape (landscape integrity and composition, the disperser community) and societal factors (previous and current land-use intensity) into account. Such a new, comprehensive framework could be tested using a combination of empirical research, experiments, process-based modelling and novel tools. Applying the framework to seres across broadscale environmental and disturbance gradients allows a better insight into what successional processes matter and under what conditions.

Lightning scars on tropical trees-Evidence and opportunities.

Lightning strikes are a significant cause of tree mortality and damage in some regions of the tropics. Formation of lightning scars on tropical trees, however, is considered rare and therefore of little relevance in identifying trees struck by lightning. Here, we suggest, based on observations made in the Bwindi Impenetrable National Park (Uganda), that lightning scars can be frequent and may be a useful diagnostic feature to aid in identifying trees struck by lightning.

Warming, drought, and disturbances lead to shifts in functional composition: A millennial-scale analysis for Amazonian and Andean sites.

Tropical forests are changing in composition and productivity, probably in response to changes in climate and disturbances. The responses to these multiple environmental drivers, and the mechanisms underlying the changes, remain largely unknown. Here, we use a functional trait approach on timescales of 10,000 years to assess how climate and disturbances influence the community-mean adult height, leaf area, seed mass, and wood density for eight lowland and highland forest landscapes. To do so, we combine data of eight fossil pollen records with functional traits and proxies for climate (temperature, precipitation, and El Niño frequency) and disturbances (fire and general disturbances). We found that temperature and disturbances were the most important drivers of changes in functional composition. Increased water availability (high precipitation and low El Niño frequency) generally led to more acquisitive trait composition (large leaves and soft wood). In lowland forests, warmer climates decreased community-mean height probably because of increased water stress, whereas in highland forests warmer climates increased height probably because of upslope migration of taller species. Disturbance increased the abundance of acquisitive, disturbance-adapted taxa with small seeds for quick colonization of disturbed sites, large leaves for light capture, and soft wood to attain fast height growth. Fire had weak effects on lowland forests but led to more stress-adapted taxa that are tall with fast life cycles and small seeds that can quickly colonize burned sites. Site-specific analyses were largely in line with cross-site analyses, except for varying site-level effects of El Niño frequency and fire activity, possibly because regional patterns in El Niño are not a good predictor of local changes, and charcoal abundances do not reflect fire intensity or severity. With future global changes, tropical Amazonian and Andean forests may transition toward shorter, drought- and disturbance-adapted forests in the lowlands but taller forests in the highlands.

Soil resistance and recovery during neotropical forest succession.

The recovery of soil conditions is crucial for successful ecosystem restoration and, hence, for achieving the goals of the UN Decade on Ecosystem Restoration. Here, we assess how soils resist forest conversion and agricultural land use, and how soils recover during subsequent tropical forest succession on abandoned agricultural fields. Our overarching question is how soil resistance and recovery depend on local conditions such as climate, soil type and land-use history. For 300 plots in 21 sites across the Neotropics, we used a chronosequence approach in which we sampled soils from two depths in old-growth forests, agricultural fields (i.e. crop fields and pastures), and secondary forests that differ in age (1-95 years) since abandonment. We measured six soil properties using a standardized sampling design and laboratory analyses. Soil resistance strongly depended on local conditions. Croplands and sites on high-activity clay (i.e. high fertility) show strong increases in bulk density and decreases in pH, carbon (C) and nitrogen (N) during deforestation and subsequent agricultural use. Resistance is lower in such sites probably because of a sharp decline in fine root biomass in croplands in the upper soil layers, and a decline in litter input from formerly productive old-growth forest (on high-activity clays). Soil recovery also strongly depended on local conditions. During forest succession, high-activity clays and croplands decreased most strongly in bulk density and increased in C and N, possibly because of strongly compacted soils with low C and N after cropland abandonment, and because of rapid vegetation recovery in high-activity clays leading to greater fine root growth and litter input. Furthermore, sites at low precipitation decreased in pH, whereas sites at high precipitation increased in N and decreased in C : N ratio. Extractable phosphorus (P) did not recover during succession, suggesting increased P limitation as forests age. These results indicate that no single solution exists for effective soil restoration and that local site conditions should determine the restoration strategies. This article is part of the theme issue 'Understanding forest landscape restoration: reinforcing scientific foundations for the UN Decade on Ecosystem Restoration'.

Multidimensional tropical forest recovery.

Tropical forests disappear rapidly because of deforestation, yet they have the potential to regrow naturally on abandoned lands. We analyze how 12 forest attributes recover during secondary succession and how their recovery is interrelated using 77 sites across the tropics. Tropical forests are highly resilient to low-intensity land use; after 20 years, forest attributes attain 78% (33 to 100%) of their old-growth values. Recovery to 90% of old-growth values is fastest for soil (<1 decade) and plant functioning (<2.5 decades), intermediate for structure and species diversity (2.5 to 6 decades), and slowest for biomass and species composition (>12 decades). Network analysis shows three independent clusters of attribute recovery, related to structure, species diversity, and species composition. Secondary forests should be embraced as a low-cost, natural solution for ecosystem restoration, climate change mitigation, and biodiversity conservation.

Forest structure drives changes in light heterogeneity during tropical secondary forest succession.

Light is a key resource for tree performance and hence, tree species partition spatial and temporal gradients in light availability. Although light distribution drives tree performance and species replacement during secondary forest succession, we yet lack understanding how light distribution changes with tropical forest development.This study aims to evaluate how changes in forest structure lead to changes in vertical and horizontal light heterogeneity during tropical forest succession.We described successional patterns in light using a chronosequence approach in which we compared 14 Mexican secondary forest stands that differ in age (8-32 years) since agricultural abandonment. For each stand, we measured vertical light profiles in 16 grid cells, and structural parameters (diameter at breast height, height and crown dimensions) for each tree.During succession, we found a rapid increase in stand size (basal area, crown area and length) and stand differentiation (i.e. a gradual leaf distribution along the forest profile), which leads to fast changes in light conditions and more light heterogeneity. The inflection points of the vertical light gradient (i.e. the absolute height at which 50% relative light intensity is attained) rapidly moved towards higher heights in the first 20 years, indicating that larger amounts of light are intercepted by canopy trees. Light attenuation rate (i.e. the rate of light extinction) decreased during succession due to slower accumulation of the crown area with height. Understorey light intensity and heterogeneity slightly decreased during succession because of an increase in crown size and a decrease in lateral gap frequency. Understorey relative light intensity was 1.56% at 32 years after abandonment.Synthesis. During succession, light conditions changed linearly, which should lead to a continuous and constant replacement of species. Especially in later successional stages, stronger vertical light gradients can limit the regeneration of light-demanding pioneer species and increase the proportion of shade-tolerant late-successional species under the canopy. These changes in light conditions were largely driven by the successional changes in forest structure, as basal area strongly determined the height where most light is absorbed, whereas crown area, and to a lesser extent crown length, determined light distribution.

Similar factors underlie tree abundance in forests in native and alien ranges.

AIM: Alien plant species can cause severe ecological and economic problems, and therefore attract a lot of research interest in biogeography and related fields. To identify potential future invasive species, we need to better understand the mechanisms underlying the abundances of invasive tree species in their new ranges, and whether these mechanisms differ between their native and alien ranges. Here, we test two hypotheses: that greater relative abundance is promoted by (a) functional difference from locally co-occurring trees, and (b) higher values than locally co-occurring trees for traits linked to competitive ability. LOCATION: Global. TIME PERIOD: Recent. MAJOR TAXA STUDIED: Trees. METHODS: We combined three global plant databases: sPlot vegetation-plot database, TRY plant trait database and Global Naturalized Alien Flora (GloNAF) database. We used a hierarchical Bayesian linear regression model to assess the factors associated with variation in local abundance, and how these relationships vary between native and alien ranges and depend on species' traits. RESULTS: In both ranges, species reach highest abundance if they are functionally similar to co-occurring species, yet are taller and have higher seed mass and wood density than co-occurring species. MAIN CONCLUSIONS: Our results suggest that light limitation leads to strong environmental and biotic filtering, and that it is advantageous to be taller and have denser wood. The striking similarities in abundance between native and alien ranges imply that information from tree species' native ranges can be used to predict in which habitats introduced species may become dominant.

Liana species decline in Congo basin contrasts with global patterns.

Lianas, woody climbing plants, are increasing in many tropical forests, with cascading effects such as decreased forest productivity, carbon sequestration, and resilience. Possible causes are increasing forest fragmentation, CO2 fertilization, and drought. Determining the primary changing species and their underlying vital rates help explain the liana trends. We monitored over 17,000 liana stems for 13 yr in 20 ha of old-growth forest in the Congo Basin, and here we report changes and vital rates for the community and for the 87 most abundant species. The total liana abundance declined from 15,007 lianas in 1994 to 11,090 in 2001 to 9,978 in 2007. Over half (52%) of the evaluated species have significantly declining populations, showing that the community response is not the result of changes in a few dominant species only. Species density change (i.e., the change in number of individuals per hectare) decreased with mortality rate, tended to increase with recruitment rate, but was independent of growth rate. Species change was independent of functional characteristics important for plant responses to fragmentation, CO2 , and drought, such as lifetime light requirements, climbing and dispersal mechanism, and leaf size. These results indicate that in Congo lianas do not show the reputed global liana increase, but rather a decline, and that elements of the reputed drivers underlying global liana change do not apply to this DR Congo forest. We suggest warfare in the Congo Basin to have decimated the elephant population, leading to less disturbance, forest closure, and declining liana numbers. Our results imply that, in this tropical forest, local causes (i.e., disturbance) override more global causes of liana change resulting in liana decline, which sharply contrasts with the liana increase observed elsewhere.

A 7000-year history of changing plant trait composition in an Amazonian landscape; the role of humans and climate.

Tropical forests are shifting in species and trait composition, but the main underlying causes remain unclear because of the short temporal scales of most studies. Here, we develop a novel approach by linking functional trait data with 7000 years of forest dynamics from a fossil pollen record of Lake Sauce in the Peruvian Amazon. We evaluate how climate and human disturbances affect community trait composition. We found weak relationships between environmental conditions and traits at the taxon level, but strong effects for community-mean traits. Overall, community-mean traits were more responsive to human disturbances than to climate change; human-induced erosion increased the dominance of dense-wooded, non-zoochorous species with compound leaves, and human-induced fire increased the dominance of tall, zoochorous taxa with large seeds and simple leaves. This information can help to enhance our understanding of forest responses to past environmental changes, and improve predictions of future changes in tropical forest composition.

The hydraulic efficiency-safety trade-off differs between lianas and trees.

Hydraulic traits are important for woody plant functioning and distribution. Associations among hydraulic traits, other leaf and stem traits, and species' performance are relatively well understood for trees, but remain poorly studied for lianas. We evaluated the coordination among hydraulic efficiency (i.e., maximum hydraulic conductivity), hydraulic safety (i.e., cavitation resistance), a suite of eight morphological and physiological traits, and species' abundances for saplings of 24 liana species and 27 tree species in wet tropical forests in Panama. Trees showed a strong trade-off between hydraulic efficiency and hydraulic safety, whereas efficiency and safety were decoupled in lianas. Hydraulic efficiency was strongly and similarly correlated with acquisitive traits for lianas and trees (e.g., positively with gas exchange rates and negatively with wood density). Hydraulic safety, however, showed no correlations with other traits in lianas, but with several in trees (e.g., positively with leaf dry matter content and wood density and negatively with gas exchange rates), indicating that in lianas hydraulic efficiency is an anchor trait because it is correlated with many other traits, while in trees both efficiency and safety are anchor traits. Traits related to shade tolerance (e.g., low specific leaf area and high wood density) were associated with high local tree sapling abundance, but not with liana abundance. Our results suggest that different, yet unknown mechanisms determine hydraulic safety and local-scale abundance for lianas compared to trees. For trees, the trade-off between efficiency and safety will provide less possibilities for ecological strategies. For lianas, however, the uncoupling of efficiency and safety could allow them to have high hydraulic efficiency, and hence high growth rates, without compromising resistance to cavitation under drought, thus allowing them to thrive and outperform trees under drier conditions.

Explaining biomass growth of tropical canopy trees: the importance of sapwood.

Tropical forests are important in worldwide carbon (C) storage and sequestration. C sequestration of these forests may especially be determined by the growth of canopy trees. However, the factors driving variation in growth among such large individuals remain largely unclear. We evaluate how crown traits [total leaf area, specific leaf area and leaf nitrogen (N) concentration] and stem traits [sapwood area (SA) and sapwood N concentration] measured for individual trees affect absolute biomass growth for 43 tropical canopy trees belonging to four species, in a moist forest in Bolivia. Biomass growth varied strongly among trees, between 17.3 and 367.3 kg year(-1), with an average of 105.4 kg year(-1). We found that variation in biomass growth was chiefly explained by a positive effect of SA, and not by tree size or other traits examined. SA itself was positively associated with sapwood growth, sapwood lifespan and basal area. We speculate that SA positively affects the growth of individual trees mainly by increasing water storage, thus securing water supply to the crown. These positive roles of sapwood on growth apparently offset the increased respiration costs incurred by more sapwood. This is one of the first individual-based studies to show that variation in sapwood traits-and not crown traits-explains variation in growth among tropical canopy trees. Accurate predictions of C dynamics in tropical forests require similar studies on biomass growth of individual trees as well as studies evaluating the dual effect of sapwood (water provision vs. respiratory costs) on tropical tree growth.

Are lianas more drought-tolerant than trees? A test for the role of hydraulic architecture and other stem and leaf traits.

Lianas are an important component of neotropical forests, where evidence suggests that they are increasing in abundance and biomass. Lianas are especially abundant in seasonally dry tropical forests, and as such it has been hypothesized that they are better adapted to drought, or that they are at an advantage under the higher light conditions in these forests. However, the physiological and morphological characteristics that allow lianas to capitalize more on seasonal forest conditions compared to trees are poorly understood. Here, we evaluate how saplings of 21 tree and liana species from a seasonal tropical forest in Panama differ in cavitation resistance (P50) and maximum hydraulic conductivity (K(h)), and how saplings of 24 tree and liana species differ in four photosynthetic leaf traits (e.g., maximum assimilation and stomatal conductance) and six morphological leaf and stem traits (e.g., wood density, maximum vessel length, and specific leaf area). At the sapling stage, lianas had a lower cavitation resistance than trees, implying lower drought tolerance, and they tended to have a higher potential hydraulic conductivity. In contrast to studies focusing on adult trees and lianas, we found no clear differences in morphological and photosynthetic traits between the life forms. Possibly, lianas and trees are functionally different at later ontogenetic stages, with lianas having deeper root systems than trees, or experience their main growth advantage during wet periods, when they are less vulnerable to cavitation and can achieve high conductivity. This study shows, however, that the hydraulic characteristics and functional traits that we examined do not explain differences in liana and tree distributions in seasonal forests.