Unveiling African rainforest composition and vulnerability to global change.

Africa is forecasted to experience large and rapid climate change1 and population growth2 during the twenty-first century, which threatens the world's second largest rainforest. Protecting and sustainably managing these African forests requires an increased understanding of their compositional heterogeneity, the environmental drivers of forest composition and their vulnerability to ongoing changes. Here, using a very large dataset of 6 million trees in more than 180,000 field plots, we jointly model the distribution in abundance of the most dominant tree taxa in central Africa, and produce continuous maps of the floristic and functional composition of central African forests. Our results show that the uncertainty in taxon-specific distributions averages out at the community level, and reveal highly deterministic assemblages. We uncover contrasting floristic and functional compositions across climates, soil types and anthropogenic gradients, with functional convergence among types of forest that are floristically dissimilar. Combining these spatial predictions with scenarios of climatic and anthropogenic global change suggests a high vulnerability of the northern and southern forest margins, the Atlantic forests and most forests in the Democratic Republic of the Congo, where both climate and anthropogenic threats are expected to increase sharply by 2085. These results constitute key quantitative benchmarks for scientists and policymakers to shape transnational conservation and management strategies that aim to provide a sustainable future for central African forests.

Interactions between soil and other environmental variables modulate forest expansion and ecotone dynamics in humid savannas of Central Africa.

Forest expansion into savanna is a pervasive phenomenon in West and Central Africa, warranting comparative studies under diverse environmental conditions. We collected vegetation data from the woody and grassy components within 73 plots of 0.16 ha distributed along a successional gradient from humid savanna to forest in Central Africa. We associated spatially collocated edaphic parameters and fire frequency derived from remote sensing to investigate their combined influence on the vegetation. Soil texture was more influential in shaping savanna structure and species distribution than soil fertility, with clay-rich soils promoting higher grass productivity and fire frequency. Savanna featuring woody aboveground biomass surpassing 40 Mg ha-1 could escape the grass-fire feedback loop, by depressing grass biomass below 4 Mg ha-1. This thicker woody layer also favoured the establishment of fire-tolerant forest pioneers, which synergically contributed to the expansion of forests. Conversely, savannas below this fire suppression threshold sustained a balance between trees and grasses through the grass-fire feedback mechanism. This hysteresis loop, particularly pronounced on clayey soils, suggests that the contrast between grassy savanna and young forests might represent alternative ecosystem states, although savannas with low woody biomass remained vulnerable to forest edge encroachment.

Climatic niche lability but growth form conservatism in the African woody flora.

Climatic niche evolution during the diversification of tropical plants has received little attention in Africa. To address this, we characterised the climatic niche of >4000 tropical African woody species, distinguishing two broad bioclimatic groups (forest vs. savanna) and six subgroups. We quantified niche conservatism versus lability at the genus level and for higher clades, using a molecular phylogeny of >800 genera. Although niche stasis at speciation is prevalent, numerous clades individually cover vast climatic spaces suggesting a general ease in transcending ecological limits, especially across bioclimatic subgroups. The forest biome was the main source of diversity, providing many lineages to savanna, but reverse shifts also occurred. We identified clades that diversified in savanna after shifts from forest. The forest-savanna transition was not consistently associated with a growth form change, though we found evolutionarily labile clades whose presence in forest or savanna is associated respectively with climbing or shrubby species diversification.

Cradles and museums of generic plant diversity across tropical Africa.

Determining where species diversify (cradles) and persist (museums) over evolutionary time is fundamental to understanding the distribution of biodiversity and for conservation prioritization. Here, we identify cradles and museums of angiosperm generic diversity across tropical Africa, one of the most biodiverse regions on Earth. Regions containing nonrandom concentrations of young (neo-) and old (paleo-) endemic taxa were identified using distribution data of 1719 genera combined with a newly generated time-calibrated mega-phylogenetic tree. We then compared the identified regions with the current network of African protected areas (PAs). At the generic level, phylogenetic diversity and endemism are mainly concentrated in the biogeographically complex region of Eastern Africa. We show that mountainous areas are centres of both neo- and paleo-endemism. By contrast, the Guineo-Congolian lowland rain forest region is characterized by widespread and old lineages. We found that the overlap between centres of phylogenetic endemism and PAs is high (> 85%). We show the vital role played by mountains acting simultaneously as cradles and museums of tropical African plant biodiversity. By contrast, lowland rainforests act mainly as museums for generic diversity. Our study shows that incorporating large-scale taxonomically verified distribution datasets and mega-phylogenies lead to an improved understanding of tropical plant biodiversity evolution.

Plastome phylogeography in two African rain forest legume trees reveals that Dahomey Gap populations originate from the Cameroon volcanic line.

Paleo-environmental data show that the distribution of African rain forests was affected by Quaternary climate changes. In particular, the Dahomey Gap (DG) - a 200 km wide savanna corridor currently separating the West African and Central African rain forest blocks and containing relict rain forest fragments - was forested during the mid-Holocene and possibly during previous interglacial periods, whereas it was dominated by open vegetation (savanna) during glacial periods. Genetic signatures of past population fragmentation and demographic changes have been found in some African forest plant species using nuclear markers, but such events appear not to have been synchronous or shared across species. To better understand the colonization history of the DG by rain forest trees through seed dispersal, the plastid genomes of two widespread African forest legume trees, Anthonotha macrophylla and Distemonanthus benthamianus, were sequenced in 47 individuals for each species, providing unprecedented phylogenetic resolution of their maternal lineages (857 and 115 SNPs, respectively). Both species exhibit distinct lineages separating three regions: 1. Upper Guinea (UG, i.e. the West African forest block), 2. the area ranging from the DG to the Cameroon volcanic line (CVL), and 3. Lower Guinea (LG, the western part of the Central African forest block) where three lineages co-occur. In both species, the DG populations (including southern Nigeria west of Cross River) exhibit much lower genetic diversity than UG and LG populations, and their plastid lineages originate from the CVL, confirming the role of the CVL as an ancient forest refuge. Despite the similar phylogeographic structures displayed by A. macrophylla and D. benthamianus, molecular dating indicates very contrasting ages of lineage divergence (UG diverged from LG since c. 7 Ma and 0.7 Ma, respectively) and DG colonization (probably following the Mid Pleistocene Transition and the Last Glacial Maximum, respectively). The stability of forest refuge areas and repeated similar forest shrinking/expanding events during successive glacial periods might explain why similar phylogeographic patterns can be generated over contrasting timescales.

An estimate of the number of tropical tree species.

The high species richness of tropical forests has long been recognized, yet there remains substantial uncertainty regarding the actual number of tropical tree species. Using a pantropical tree inventory database from closed canopy forests, consisting of 657,630 trees belonging to 11,371 species, we use a fitted value of Fisher's alpha and an approximate pantropical stem total to estimate the minimum number of tropical forest tree species to fall between ∼ 40,000 and ∼ 53,000, i.e., at the high end of previous estimates. Contrary to common assumption, the Indo-Pacific region was found to be as species-rich as the Neotropics, with both regions having a minimum of ∼ 19,000-25,000 tree species. Continental Africa is relatively depauperate with a minimum of ∼ 4,500-6,000 tree species. Very few species are shared among the African, American, and the Indo-Pacific regions. We provide a methodological framework for estimating species richness in trees that may help refine species richness estimates of tree-dependent taxa.

Exploring the floristic diversity of tropical Africa.

BACKGROUND: Understanding the patterns of biodiversity distribution and what influences them is a fundamental pre-requisite for effective conservation and sustainable utilisation of biodiversity. Such knowledge is increasingly urgent as biodiversity responds to the ongoing effects of global climate change. Nowhere is this more acute than in species-rich tropical Africa, where so little is known about plant diversity and its distribution. In this paper, we use RAINBIO - one of the largest mega-databases of tropical African vascular plant species distributions ever compiled - to address questions about plant and growth form diversity across tropical Africa. RESULTS: The filtered RAINBIO dataset contains 609,776 georeferenced records representing 22,577 species. Growth form data are recorded for 97% of all species. Records are well distributed, but heterogeneous across the continent. Overall, tropical Africa remains poorly sampled. When using sampling units (SU) of 0.5°, just 21 reach appropriate collection density and sampling completeness, and the average number of records per species per SU is only 1.84. Species richness (observed and estimated) and endemism figures per country are provided. Benin, Cameroon, Gabon, Ivory Coast and Liberia appear as the botanically best-explored countries, but none are optimally explored. Forests in the region contain 15,387 vascular plant species, of which 3013 are trees, representing 5-7% of the estimated world's tropical tree flora. The central African forests have the highest endemism rate across Africa, with approximately 30% of species being endemic. CONCLUSIONS: The botanical exploration of tropical Africa is far from complete, underlining the need for intensified inventories and digitization. We propose priority target areas for future sampling efforts, mainly focused on Tanzania, Atlantic Central Africa and West Africa. The observed number of tree species for African forests is smaller than those estimated from global tree data, suggesting that a significant number of species are yet to be discovered. Our data provide a solid basis for a more sustainable management and improved conservation of tropical Africa's unique flora, and is important for achieving Objective 1 of the Global Strategy for Plant Conservation 2011-2020. In turn, RAINBIO provides a solid basis for a more sustainable management and improved conservation of tropical Africa's unique flora.

Pleistocene population expansions of shade-tolerant trees indicate fragmentation of the African rainforest during the Ice Ages.

The fossil record in tropical Africa suggests that dry conditions during the Ice Ages caused expansion of savannahs and contraction of the rainforest. Forest refugia have been proposed to be located in areas of Central Africa that currently harbour high rates of endemic species. However, to what extent the forest was fragmented remains unknown. Nuclear microsatellites and plastid sequences of 732 trees of two species occurring in the same habitat-mature lowland evergreen rainforests-but with remarkably different dispersal capacities-animal versus gravity-were analysed. Geographical information system tools revealed intraspecific lineages partially congruent across the two species, suggesting common past barriers to gene flow in Central Africa. According to approximate Bayesian computation, the intraspecific genetic clusters diverged during the Pleistocene (less than 2 Ma), so that intraspecific differentiation is the appropriate scale to test the aridification effect of the Ice Ages on tree populations. Demographic tests revealed clear genetic signals of population expansion in both taxa, possibly following bottleneck events after forest fragmentation, with stronger evidence of expansion after the Penultimate rather than after the Last Glacial Maximum. The differential dispersal capacity may have modulated the particular response of each species to climate change, as revealed by the stronger evidence of expansion found in the animal-dispersed species than in the gravity-dispersed one.

Widespread introduced species dominate the urban tree assemblage on the endemic-rich tropical island of São Tomé.

The Afrotropics are experiencing some of the fastest urbanisation rates on the planet but the impact of city growth on their rich and unique biodiversity remains understudied, especially compared to natural baselines. Little is also known about how introduced species influence ß-diversity in these contexts, and how patterns coincide with native ranges of species. Here we investigated how tree assemblages of the endemic-rich Afrotropical island of São Tomé differed between urban, rural and natural zones. These were primarily characterised by urban greenspaces, shade plantations, and old-growth forests, respectively. Based on 81 transects, we assessed biodiversity metrics of endemic, native and introduced species. Tree abundance and species richness were highest in the natural zone, where the composition was most different from the urban zone. The tree community of the rural zone was the most uneven and had the least variation among transects, representing the lowest ß-diversity. The urban zone was dominated by introduced species (57.7%), while the natural zone hosted almost exclusively native species (93.3%), including many endemics (26.1%). The biogeographic realms that species originated from were particularly diverse in the urban zone, with few species from the Afrotropics. In contrast to native and endemic trees, introduced trees were clearly associated with urban and rural expansion, as they were much more abundant and species-rich in these zones than in the natural zone, facilitating biotic homogenisation. These findings highlight how urban and rural environments are affecting the native tree flora of São Tomé, and the need for conservation measures geared towards globally threatened and endemic tree species. Importantly, these require the protection of natural forests, despite the rising land demands for settlements and agriculture. Ultimately, such action to conserve endemic trees will contribute to global efforts to prevent further biodiversity declines.

Comprehensive conservation assessments reveal high extinction risks across Atlantic Forest trees.

Biodiversity is declining globally, yet many biodiversity hotspots still lack comprehensive species conservation assessments. Using multiple International Union for Conservation of Nature (IUCN) Red List criteria to evaluate extinction risks and millions of herbarium and forest inventory records, we present automated conservation assessments for all tree species of the Atlantic Forest biodiversity hotspot, including ~1100 heretofore unassessed species. About 65% of all species and 82% of endemic species are classified as threatened. We rediscovered five species classified as Extinct on the IUCN Red List and identified 13 endemics as possibly extinct. Uncertainties in species information had little influence on the assessments, but using fewer Red List criteria severely underestimated threat levels. We suggest that the conservation status of tropical forests worldwide is worse than previously reported.

LiDAR-based reference aboveground biomass maps for tropical forests of South Asia and Central Africa.

Accurate mapping and monitoring of tropical forests aboveground biomass (AGB) is crucial to design effective carbon emission reduction strategies and improving our understanding of Earth's carbon cycle. However, existing large-scale maps of tropical forest AGB generated through combinations of Earth Observation (EO) and forest inventory data show markedly divergent estimates, even after accounting for reported uncertainties. To address this, a network of high-quality reference data is needed to calibrate and validate mapping algorithms. This study aims to generate reference AGB datasets using field inventory plots and airborne LiDAR data for eight sites in Central Africa and five sites in South Asia, two regions largely underrepresented in global reference AGB datasets. The study provides access to these reference AGB maps, including uncertainty maps, at 100 m and 40 m spatial resolutions covering a total LiDAR footprint of 1,11,650 ha [ranging from 150 to 40,000 ha at site level]. These maps serve as calibration/validation datasets to improve the accuracy and reliability of AGB mapping for current and upcoming EO missions (viz., GEDI, BIOMASS, and NISAR).

The ECAT dataset: expert-validated distribution data of endemic and sub-endemic trees of Central Africa (Dem. Rep. Congo, Rwanda, Burundi).

In this data paper, we present a specimen-based occurrence dataset compiled in the framework of the Conservation of Endemic Central African Trees (ECAT) project with the aim of producing global conservation assessments for the IUCN Red List. The project targets all tree species endemic or sub-endemic to the Central African region comprising the Democratic Republic of the Congo (DR Congo), Rwanda, and Burundi. The dataset contains 6361 plant collection records with occurrences of 8910 specimens from 337 taxa belonging to 153 genera in 52 families. Many of these tree taxa have restricted geographic ranges and are only known from a small number of herbarium specimens. As assessments for such taxa can be compromised by inadequate data, we transcribed and geo-referenced specimen label information to obtain a more accurate and complete locality dataset. All specimen data were manually cleaned and verified by botanical experts, resulting in improved data quality and consistency.

Development and characterization of microsatellite loci in Pericopsis elata (Fabaceae) using a cost-efficient approach.

PREMISE OF THE STUDY: Microsatellite loci were developed in the endangered Pericopsis elata using a combination of low-cost procedures. METHODS AND RESULTS: Microsatellite isolation was performed simultaneously on three distinct species through a newly available procedure that associates multiplex microsatellite enrichment and next-generation sequencing, allowing the rapid and low-cost development of microsatellite-enriched libraries through the use of a 1/32nd GS-FLX plate. Genotyping using M13-like labeling in multiplexed reactions allowed additional cost savings. From 72 primers selected for initial screening, 21 positively amplified P. elata, and 11 showed polymorphism with two to 11 alleles per locus and a mean value of 5.4 alleles per locus. CONCLUSIONS: These microsatellite loci will be useful to further investigate the level of genetic variation within and between natural populations of P. elata in Africa.

Tectonics, climate and the diversification of the tropical African terrestrial flora and fauna.

Tropical Africa is home to an astonishing biodiversity occurring in a variety of ecosystems. Past climatic change and geological events have impacted the evolution and diversification of this biodiversity. During the last two decades, around 90 dated molecular phylogenies of different clades across animals and plants have been published leading to an increased understanding of the diversification and speciation processes generating tropical African biodiversity. In parallel, extended geological and palaeoclimatic records together with detailed numerical simulations have refined our understanding of past geological and climatic changes in Africa. To date, these important advances have not been reviewed within a common framework. Here, we critically review and synthesize African climate, tectonics and terrestrial biodiversity evolution throughout the Cenozoic to the mid-Pleistocene, drawing on recent advances in Earth and life sciences. We first review six major geo-climatic periods defining tropical African biodiversity diversification by synthesizing 89 dated molecular phylogeny studies. Two major geo-climatic factors impacting the diversification of the sub-Saharan biota are highlighted. First, Africa underwent numerous climatic fluctuations at ancient and more recent timescales, with tectonic, greenhouse gas, and orbital forcing stimulating diversification. Second, increased aridification since the Late Eocene led to important extinction events, but also provided unique diversification opportunities shaping the current tropical African biodiversity landscape. We then review diversification studies of tropical terrestrial animal and plant clades and discuss three major models of speciation: (i) geographic speciation via vicariance (allopatry); (ii) ecological speciation impacted by climate and geological changes, and (iii) genomic speciation via genome duplication. Geographic speciation has been the most widely documented to date and is a common speciation model across tropical Africa. We conclude with four important challenges faced by tropical African biodiversity research: (i) to increase knowledge by gathering basic and fundamental biodiversity information; (ii) to improve modelling of African geophysical evolution throughout the Cenozoic via better constraints and downscaling approaches; (iii) to increase the precision of phylogenetic reconstruction and molecular dating of tropical African clades by using next generation sequencing approaches together with better fossil calibrations; (iv) finally, as done here, to integrate data better from Earth and life sciences by focusing on the interdisciplinary study of the evolution of tropical African biodiversity in a wider geodiversity context.

A large-scale species level dated angiosperm phylogeny for evolutionary and ecological analyses.

Phylogenies are a central and indispensable tool for evolutionary and ecological research. Even though most angiosperm families are well investigated from a phylogenetic point of view, there are far less possibilities to carry out large-scale meta-analyses at order level or higher. Here, we reconstructed a large-scale dated phylogeny including nearly 1/8th of all angiosperm species, based on two plastid barcoding genes, matK (incl. trnK) and rbcL. Novel sequences were generated for several species, while the rest of the data were mined from GenBank. The resulting tree was dated using 56 angiosperm fossils as calibration points. The resulting megaphylogeny is one of the largest dated phylogenetic tree of angiosperms yet, consisting of 36,101 sampled species, representing 8,399 genera, 426 families and all orders. This novel framework will be useful for investigating different broad scale research questions in ecological and evolutionary biology.

The commonness of rarity: Global and future distribution of rarity across land plants.

A key feature of life's diversity is that some species are common but many more are rare. Nonetheless, at global scales, we do not know what fraction of biodiversity consists of rare species. Here, we present the largest compilation of global plant diversity to quantify the fraction of Earth's plant biodiversity that are rare. A large fraction, ~36.5% of Earth's ~435,000 plant species, are exceedingly rare. Sampling biases and prominent models, such as neutral theory and the k-niche model, cannot account for the observed prevalence of rarity. Our results indicate that (i) climatically more stable regions have harbored rare species and hence a large fraction of Earth's plant species via reduced extinction risk but that (ii) climate change and human land use are now disproportionately impacting rare species. Estimates of global species abundance distributions have important implications for risk assessments and conservation planning in this era of rapid global change.

Taxonomic revision of the African genus Greenwayodendron (Annonaceae).

Greenwayodendron (Annonaceae) is a tropical African genus of trees occurring mainly in rain forests. Until recently, Greenwayodendron contained only two species: Greenwayodendronoliveri from West Africa and Greenwayodendronsuaveolens from Central and East Africa. Genetic data, using chloroplast haplotypes and nuclear microsatellites as well as morphometric analyses, provided important information on the delineation of species. Greenwayodendron now contains six species, including two new species (Greenwayodendronglabrum Lissambou, Hardy & Couvreur, sp. nov. and Greenwayodendronlittorale Lissambou, Dauby & Couvreur, sp. nov.). Greenwayodendronsuaveolensvar.gabonica and Greenwayodendronsuaveolenssubsp.usambaricum are recognised as distinct species: Greenwayodendrongabonicum comb. nov. and Greenwayodendronusambaricum comb. nov., respectively. A key, detailed descriptions of morphology and geographic distributions, as well as notes on their ecology and uses are presented for all species. Preliminary conservation assessments following IUCN criteria are also provided. Two species are preliminarily identified as threatened, one as Endangered and one as Vulnerable.

ConR: An R package to assist large-scale multispecies preliminary conservation assessments using distribution data.

The Red List Categories and the accompanying five criteria developed by the International Union for Conservation of Nature (IUCN) provide an authoritative and comprehensive methodology to assess the conservation status of organisms. Red List criterion B, which principally uses distribution data, is the most widely used to assess conservation status, particularly of plant species. No software package has previously been available to perform large-scale multispecies calculations of the three main criterion B parameters [extent of occurrence (EOO), area of occupancy (AOO) and an estimate of the number of locations] and provide preliminary conservation assessments using an automated batch process. We developed ConR, a dedicated R package, as a rapid and efficient tool to conduct large numbers of preliminary assessments, thereby facilitating complete Red List assessment. ConR (1) calculates key geographic range parameters (AOO and EOO) and estimates the number of locations sensu IUCN needed for an assessment under criterion B; (2) uses this information in a batch process to generate preliminary assessments of multiple species; (3) summarize the parameters and preliminary assessments in a spreadsheet; and (4) provides a visualization of the results by generating maps suitable for the submission of full assessments to the IUCN Red List. ConR can be used for any living organism for which reliable georeferenced distribution data are available. As distributional data for taxa become increasingly available via large open access datasets, ConR provides a novel, timely tool to guide and accelerate the work of the conservation and taxonomic communities by enabling practitioners to conduct preliminary assessments simultaneously for hundreds or even thousands of species in an efficient and time-saving way.

RAINBIO: a mega-database of tropical African vascular plants distributions.

The tropical vegetation of Africa is characterized by high levels of species diversity but is undergoing important shifts in response to ongoing climate change and increasing anthropogenic pressures. Although our knowledge of plant species distribution patterns in the African tropics has been improving over the years, it remains limited. Here we present RAINBIO, a unique comprehensive mega-database of georeferenced records for vascular plants in continental tropical Africa. The geographic focus of the database is the region south of the Sahel and north of Southern Africa, and the majority of data originate from tropical forest regions. RAINBIO is a compilation of 13 datasets either publicly available or personal ones. Numerous in depth data quality checks, automatic and manual via several African flora experts, were undertaken for georeferencing, standardization of taxonomic names and identification and merging of duplicated records. The resulting RAINBIO data allows exploration and extraction of distribution data for 25,356 native tropical African vascular plant species, which represents ca. 89% of all known plant species in the area of interest. Habit information is also provided for 91% of these species.

Comparative phylogeography in rainforest trees from Lower Guinea, Africa.

Comparative phylogeography is an effective approach to assess the evolutionary history of biological communities. We used comparative phylogeography in fourteen tree taxa from Lower Guinea (Atlantic Equatorial Africa) to test for congruence with two simple evolutionary scenarios based on physio-climatic features 1) the W-E environmental gradient and 2) the N-S seasonal inversion, which determine climatic and seasonality differences in the region. We sequenced the trnC-ycf6 plastid DNA region using a dual sampling strategy: fourteen taxa with small sample sizes (dataset 1, mean n = 16/taxon), to assess whether a strong general pattern of allele endemism and genetic differentiation emerged; and four taxonomically well-studied species with larger sample sizes (dataset 2, mean n = 109/species) to detect the presence of particular shared phylogeographic patterns. When grouping the samples into two alternative sets of two populations, W and E, vs. N and S, neither dataset exhibited a strong pattern of allelic endemism, suggesting that none of the considered regions consistently harboured older populations. Differentiation in dataset 1 was similarly strong between W and E as between N and S, with 3-5 significant F ST tests out of 14 tests in each scenario. Coalescent simulations indicated that, given the power of the data, this result probably reflects idiosyncratic histories of the taxa, or a weak common differentiation pattern (possibly with population substructure) undetectable across taxa in dataset 1. Dataset 2 identified a common genetic break separating the northern and southern populations of Greenwayodendron suaveolens subsp. suaveolens var. suaveolens, Milicia excelsa, Symphonia globulifera and Trichoscypha acuminata in Lower Guinea, in agreement with differentiation across the N-S seasonal inversion. Our work suggests that currently recognized tree taxa or suspected species complexes can contain strongly differentiated genetic lineages, which could lead to misinterpretation of phylogeographic patterns. Therefore the evolutionary processes of such taxa require further study in African tropical rainforests.