Southeast Asian Dipterocarp origin and diversification driven by Africa-India floristic interchange.

The evolution and diversification of ancient megathermal angiosperm lineages with Africa-India origins in Asian tropical forests is poorly understood because of the lack of reliable fossils. Our palaeobiogeographical analysis of pollen fossils from Africa and India combined with molecular data and fossil amber records suggest a tropical-African origin of Dipterocarpaceae during the mid-Cretaceous and its dispersal to India during the Late Maastrichtian and Paleocene, leading to range expansion of aseasonal dipterocarps on the Indian Plate. The India-Asia collision further facilitated the dispersal of dipterocarps from India to similar climatic zones in Southeast Asia, which supports their out-of-India migration. The dispersal pathway suggested for Dipterocarpaceae may provide a framework for an alternative biogeographic hypothesis for several megathermal angiosperm families that are presently widely distributed in Southeast Asia.

The interspecific growth-mortality trade-off is not a general framework for tropical forest community structure.

Resource allocation within trees is a zero-sum game. Unavoidable trade-offs dictate that allocation to growth-promoting functions curtails other functions, generating a gradient of investment in growth versus survival along which tree species align, known as the interspecific growth-mortality trade-off. This paradigm is widely accepted but not well established. Using demographic data for 1,111 tree species across ten tropical forests, we tested the generality of the growth-mortality trade-off and evaluated its underlying drivers using two species-specific parameters describing resource allocation strategies: tolerance of resource limitation and responsiveness of allocation to resource access. Globally, a canonical growth-mortality trade-off emerged, but the trade-off was strongly observed only in less disturbance-prone forests, which contained diverse resource allocation strategies. Only half of disturbance-prone forests, which lacked tolerant species, exhibited the trade-off. Supported by a theoretical model, our findings raise questions about whether the growth-mortality trade-off is a universally applicable organizing framework for understanding tropical forest community structure.

Molecular phylogenomics of the tribe Shoreeae (Dipterocarpaceae) using whole plastid genomes.

BACKGROUND AND AIMS: Phylogenetic relationships within tribe Shoreeae, containing the main elements of tropical forests in Southeast Asia, present a long-standing problem in the systematics of Dipterocarpaceae. Sequencing whole plastomes using next-generation sequencing- (NGS) based genome skimming is increasingly employed for investigating phylogenetic relationships of plants. Here, the usefulness of complete plastid genome sequences in resolving phylogenetic relationships within Shoreeae is evaluated. METHODS: A pipeline to obtain alignments of whole plastid genome sequences across individuals with different amounts of available data is presented. In total, 48 individuals, representing 37 species and four genera of the ecologically and economically important tribe Shoreeae sensu Ashton, were investigated. Phylogenetic trees were reconstructed using maximum parsimony, maximum likelihood and Bayesian inference. KEY RESULTS: Here, the first fully sequenced plastid genomes for the tribe Shoreeae are presented. Their size, GC content and gene order are comparable with those of other members of Malvales. Phylogenomic analyses demonstrate that whole plastid genomes are useful for inferring phylogenetic relationships among genera and groups of Shorea (Shoreeae) but fail to provide well-supported phylogenetic relationships among some of the most closely related species. Discordance in placement of Parashorea was observed between phylogenetic trees obtained from plastome analyses and those obtained from nuclear single nucleotide polymorphism (SNP) data sets identified in restriction-site associated sequencing (RADseq). CONCLUSIONS: Phylogenomic analyses of the entire plastid genomes are useful for inferring phylogenetic relationships at lower taxonomic levels, but are not sufficient for detailed phylogenetic reconstructions of closely related species groups in Shoreeae. Discordance in placement of Parashorea was further investigated for evidence of ancient hybridization.

Phylogenomics resolves evolutionary relationships and provides insights into floral evolution in the tribe Shoreeae (Dipterocarpaceae).

A supra-annual, community-level synchronous flowering prevails in several parts of the tropical forests of Southeast Asia and its evolution has been hypothesized to be linked to pollinator shifts. The aseasonal Southeast Asian lowland rainforests are dominated by Dipterocarpaceae, which exhibit great floral diversity, a range of pollination syndromes and include species with annual and supra-annual gregarious flowering. Phylogenetic relationships within this family are still unclear, especially in the tribe Shoreeae. Here, we develop a pipeline to maximize recovery of genome-wide SNPs from restriction-site associated DNA sequencing (RADseq) in non-model organisms across wide phylogenetic scales. We then infer phylogenomic relationships in the tribe Shoreeae using both traditional and coalescent analyses. The phylogenetic trees obtained with these methods are congruent to each other and highly resolved. They allow reconstructing the evolutionary patterns of floral traits (number of stamens, anther structure and anther/appendage size) in the group. Our inferences indicate that species with many stamens, but smaller, globose anthers and longer appendages and have evolved multiple times from species with fewer stamens, but larger, oblong anthers and shorter appendages. This could have happened in parallel to iterative shifts in pollinators across the uncovered phylogeny from larger, longer generation to smaller, shorter-generation insects that can quickly build up the necessary population sizes during mass flowering episodes.

An integrated pan-tropical biomass map using multiple reference datasets.

We combined two existing datasets of vegetation aboveground biomass (AGB) (Proceedings of the National Academy of Sciences of the United States of America, 108, 2011, 9899; Nature Climate Change, 2, 2012, 182) into a pan-tropical AGB map at 1-km resolution using an independent reference dataset of field observations and locally calibrated high-resolution biomass maps, harmonized and upscaled to 14 477 1-km AGB estimates. Our data fusion approach uses bias removal and weighted linear averaging that incorporates and spatializes the biomass patterns indicated by the reference data. The method was applied independently in areas (strata) with homogeneous error patterns of the input (Saatchi and Baccini) maps, which were estimated from the reference data and additional covariates. Based on the fused map, we estimated AGB stock for the tropics (23.4 N-23.4 S) of 375 Pg dry mass, 9-18% lower than the Saatchi and Baccini estimates. The fused map also showed differing spatial patterns of AGB over large areas, with higher AGB density in the dense forest areas in the Congo basin, Eastern Amazon and South-East Asia, and lower values in Central America and in most dry vegetation areas of Africa than either of the input maps. The validation exercise, based on 2118 estimates from the reference dataset not used in the fusion process, showed that the fused map had a RMSE 15-21% lower than that of the input maps and, most importantly, nearly unbiased estimates (mean bias 5 Mg dry mass ha(-1) vs. 21 and 28 Mg ha(-1) for the input maps). The fusion method can be applied at any scale including the policy-relevant national level, where it can provide improved biomass estimates by integrating existing regional biomass maps as input maps and additional, country-specific reference datasets.

Demographic properties shape tree size distribution in a Malaysian rain forest.

Different mechanisms have been proposed to explain how vertical and horizontal heterogeneity in light conditions enhances tree species coexistence in forest ecosystems. The foliage partitioning theory proposes that differentiation in vertical foliage distribution, caused by an interspecific variation in mortality-to-growth ratio, promotes stable coexistence. In contrast, successional niche theory posits that horizontal light heterogeneity, caused by gap dynamics, enhances species coexistence through an interspecific trade-off between growth rate and survival. To distinguish between these theories of species coexistence, we analyzed tree inventory data for 370 species from the 50-ha plot in Pasoh Forest Reserve, Malaysia. We used community-wide Bayesian models to quantify size-dependent growth rate and mortality of every species. We compared the observed size distributions and the projected distributions from size-dependent demographic rates. We found that the observed size distributions were not simply correlated with the rate of population increase but were related to demographic properties such as size growth rate and mortality. Species with low relative abundance of juveniles in size distribution showed high growth rate and low mortality at small tree sizes and low per-capita recruitment rate. Overall, our findings were in accordance with those predicted by foliage partitioning theory.

Variability in solar radiation and temperature explains observed patterns and trends in tree growth rates across four tropical forests.

The response of tropical forests to global climate variability and change remains poorly understood. Results from long-term studies of permanent forest plots have reported different, and in some cases opposing trends in tropical forest dynamics. In this study, we examined changes in tree growth rates at four long-term permanent tropical forest research plots in relation to variation in solar radiation, temperature and precipitation. Temporal variation in the stand-level growth rates measured at five-year intervals was found to be positively correlated with variation in incoming solar radiation and negatively related to temporal variation in night-time temperatures. Taken alone, neither solar radiation variability nor the effects of night-time temperatures can account for the observed temporal variation in tree growth rates across sites, but when considered together, these two climate variables account for most of the observed temporal variability in tree growth rates. Further analysis indicates that the stand-level response is primarily driven by the responses of smaller-sized trees (less than 20 cm in diameter). The combined temperature and radiation responses identified in this study provide a potential explanation for the conflicting patterns in tree growth rates found in previous studies.

Assessing evidence for a pervasive alteration in tropical tree communities.

In Amazonian tropical forests, recent studies have reported increases in aboveground biomass and in primary productivity, as well as shifts in plant species composition favouring fast-growing species over slow-growing ones. This pervasive alteration of mature tropical forests was attributed to global environmental change, such as an increase in atmospheric CO2 concentration, nutrient deposition, temperature, drought frequency, and/or irradiance. We used standardized, repeated measurements of over 2 million trees in ten large (16-52 ha each) forest plots on three continents to evaluate the generality of these findings across tropical forests. Aboveground biomass increased at seven of our ten plots, significantly so at four plots, and showed a large decrease at a single plot. Carbon accumulation pooled across sites was significant (+0.24 MgC ha(-1) y(-1), 95% confidence intervals [0.07, 0.39] MgC ha(-1) y(-1)), but lower than reported previously for Amazonia. At three sites for which we had data for multiple census intervals, we found no concerted increase in biomass gain, in conflict with the increased productivity hypothesis. Over all ten plots, the fastest-growing quartile of species gained biomass (+0.33 [0.09, 0.55] % y(-1)) compared with the tree community as a whole (+0.15 % y(-1)); however, this significant trend was due to a single plot. Biomass of slow-growing species increased significantly when calculated over all plots (+0.21 [0.02, 0.37] % y(-1)), and in half of our plots when calculated individually. Our results do not support the hypothesis that fast-growing species are consistently increasing in dominance in tropical tree communities. Instead, they suggest that our plots may be simultaneously recovering from past disturbances and affected by changes in resource availability. More long-term studies are necessary to clarify the contribution of global change to the functioning of tropical forests.

The role of gap phase processes in the biomass dynamics of tropical forests.

The responses of tropical forests to global anthropogenic disturbances remain poorly understood. Above-ground woody biomass in some tropical forest plots has increased over the past several decades, potentially reflecting a widespread response to increased resource availability, for example, due to elevated atmospheric CO2 and/or nutrient deposition. However, previous studies of biomass dynamics have not accounted for natural patterns of disturbance and gap phase regeneration, making it difficult to quantify the importance of environmental changes. Using spatially explicit census data from large (50 ha) inventory plots, we investigated the influence of gap phase processes on the biomass dynamics of four 'old-growth' tropical forests (Barro Colorado Island (BCI), Panama; Pasoh and Lambir, Malaysia; and Huai Kha Khaeng (HKK), Thailand). We show that biomass increases were gradual and concentrated in earlier-phase forest patches, while biomass losses were generally of greater magnitude but concentrated in rarer later-phase patches. We then estimate the rate of biomass change at each site independent of gap phase dynamics using reduced major axis regressions and ANCOVA tests. Above-ground woody biomass increased significantly at Pasoh (+0.72% yr(-1)) and decreased at HKK (-0.56% yr(-1)) independent of changes in gap phase but remained stable at both BCI and Lambir. We conclude that gap phase processes play an important role in the biomass dynamics of tropical forests, and that quantifying the role of gap phase processes will help improve our understanding of the factors driving changes in forest biomass as well as their place in the global carbon budget.

Contrasting structure and composition of the understory in species-rich tropical rain forests.

In large samples of trees > or = 1 cm dbh (more than 1 million trees and 3000 species), in six lowland tropical forests on three continents, we assigned species with >30 individuals to one of six classes of stature at maturity (SAM). We then compared the proportional representation of understory trees (1-2 cm dbh) among these classes. The understory of the three Asian sites was predominantly composed of the saplings of large-canopy trees whereas the African and American sites were more richly stocked with trees of the smaller SAM classes. Differences in class representation were related to taxonomic families that were present exclusively in one continent or another. Families found in the Asian plots but not in the American plot (e.g., Dipterocarpaceae, Fagaceae) were predominantly species of the largest SAM classes, whereas families exclusive to the American plots (e.g., Melastomataceae sensu stricto, Piperaceae, and Malvaceae [Bombacacoidea]) were predominantly species of small classes. The African plot was similar to Asia in the absence of those American families rich in understory species, while similar to America in lacking the Asian families rich in canopy species. The numerous understory species of Africa were chiefly derived from families shared with Asia and/or America. The ratio of saplings (1-2 cm dbh) to conspecific canopy trees (>40 cm dbh) was lower in American plots than in the Asian plots. Possible explanations for these differences include phenology, moisture and soil fertility regimes, phyletic constraints, and the role of early successional plants in forest development. These results demonstrate that tropical forests that appear similar in tree number, basal area, and the family taxonomy of canopy trees nonetheless differ in ecological structure in ways that may impact the ecology of pollinators, dispersers, and herbivores and might reflect fundamental differences in canopy tree regeneration.

Cluster analysis of spatial patterns in Malaysian tree species.

Tree species in tropical rain forests exhibit a rich panoply of spatial patterns that beg ecological explanation. The analysis of tropical census data typically relies on spatial statistics, which quantify the average aggregation tendency of a species. In this article we develop a cluster-based approach that complements traditional spatial statistics in the exploration and analysis of ecological hypotheses for spatial pattern. We apply this technique to six study species within a fully mapped 50-ha forest census in peninsular Malaysia. For each species we identify the scale(s) of spatial aggregation and the corresponding tree clusters. We study the correlation between cluster locations and abiotic variables such as topography. We find that the distribution of cluster sizes exhibits equilibrium and nonequilibrium behavior depending on species life history. The distribution of tree diameters within clusters also varies according to species life history. At different spatial scales, we find evidence for both niche-based and dispersal-limited processes producing spatial pattern. Our methodology for identifying scales of aggregation and clusters is general; we discuss the method's applicability to spatial problems outside of tropical plant ecology.