Molecular phylogeny and evolution of inflorescence types in Eperua.

PREMISE: The Amazonian hyperdominant genus Eperua (Fabaceae) currently holds 20 described species and has two strongly different inflorescence and flower types, with corresponding different pollination syndrome. The evolution of these vastly different inflorescence types within this genus was unknown and the main topic in this study. METHODS: We constructed a molecular phylogeny, based on the full nuclear ribosomal DNA and partial plastome, using Bayesian inference and maximum likelihood methods, to test whether the genus is monophyletic, whether all species are monophyletic and if the shift from bat to bee pollination (or vice versa) occurred once in this genus. RESULTS: All but two species are well supported by the nuclear ribosomal phylogeny. The plastome phylogeny, however, shows a strong geographic signal suggesting strong local hybridization or chloroplast capture, rendering chloroplast barcodes meaningless in this genus. CONCLUSIONS: With our data, we cannot fully resolve the backbone of the tree to clarify sister genera relationships and confirm monophyly of the genus Eperua. Within the genus, the shift from bat to bee and bee to bat pollination has occurred several times but, with the bee to bat not always leading to a pendant inflorescence.

Scaling issues of neutral theory reveal violations of ecological equivalence for dominant Amazonian tree species.

Neutral models are often used as null models, testing the relative importance of niche versus neutral processes in shaping diversity. Most versions, however, focus only on regional scale predictions and neglect local level contributions. Recently, a new formulation of spatial neutral theory was published showing an incompatibility between regional and local scale fits where especially the number of rare species was dramatically under-predicted. Using a forward in time semi-spatially explicit neutral model and a unique large-scale Amazonian tree inventory data set, we show that neutral theory not only underestimates the number of rare species but also fails in predicting the excessive dominance of species on both regional and local levels. We show that although there are clear relationships between species composition, spatial and environmental distances, there is also a clear differentiation between species able to attain dominance with and without restriction to specific habitats. We conclude therefore that the apparent dominance of these species is real, and that their excessive abundance can be attributed to fitness differences in different ways, a clear violation of the ecological equivalence assumption of neutral theory.

Tropical rainforests that persisted: inferences from the Quaternary demographic history of eight tree species in the Guiana shield.

How Quaternary climatic and geological disturbances influenced the composition of Neotropical forests is hotly debated. Rainfall and temperature changes during and/or immediately after the last glacial maximum (LGM) are thought to have strongly affected the geographical distribution and local abundance of tree species. The paucity of the fossil records in Neotropical forests prevents a direct reconstruction of such processes. To describe community-level historical trends in forest composition, we turned therefore to inferential methods based on the reconstruction of past demographic changes. In particular, we modelled the history of rainforests in the eastern Guiana Shield over a timescale of several thousand generations, through the application of approximate Bayesian computation and maximum-likelihood methods to diversity data at nuclear and chloroplast loci in eight species or subspecies of rainforest trees. Depending on the species and on the method applied, we detected population contraction, expansion or stability, with a general trend in favour of stability or expansion, with changes presumably having occurred during or after the LGM. These findings suggest that Guiana Shield rainforests have globally persisted, while expanding, through the Quaternary, but that different species have experienced different demographic events, with a trend towards the increase in frequency of light-demanding, disturbance-associated species.

Estimating species richness in hyper-diverse large tree communities.

Species richness estimation is one of the most widely used analyses carried out by ecologists, and nonparametric estimators are probably the most used techniques to carry out such estimations. We tested the assumptions and results of nonparametric estimators and those of a logseries approach to species richness estimation for simulated tropical forests and five data sets from the field. We conclude that nonparametric estimators are not suitable to estimate species richness in tropical forests, where sampling intensity is usually low and richness is high, because the assumptions of the methods do not meet the sampling strategy used in most studies. The logseries, while also requiring substantial sampling, is much more effective in estimating species richness than commonly used nonparametric estimators, and its assumptions better match the way field data is being collected.

Revisiting a universal airborne light detection and ranging approach for tropical forest carbon mapping: scaling-up from tree to stand to landscape.

Airborne laser scanning provides continuous coverage mapping of forest canopy height and thereby is a powerful tool to scale-up above-ground biomass (AGB) estimates from stand to landscape. A critical first step is the selection of the plot variables which can be related to light detection and ranging (LiDAR) statistics. A universal approach was previously proposed which combines local and regional estimates of basal area (BA) and wood density with LiDAR-derived canopy height to map carbon at a regional scale (Asner et al. in Oecologia 168:1147-1160, 2012). Here we explore the contribution of stem diameter distribution, specific wood density and height-diameter (H-D) allometry to forest stand AGB and propose an alternative model. By applying the new model to a large tropical forest data set we show that an appropriate choice of input variables is essential to minimize prediction error of stand AGB which will propagate at larger scale. Stem number (N) and average stem cross-sectional area should be used instead of BA when scaling from tree to plot. Stand quadratic mean diameter above the census threshold diameter size should be preferred over stand mean diameter as it reduces the prediction error of stand AGB by a factor of ten. Wood density should be weighted by stem volume per species instead of BA. LiDAR-derived statistics should prove useful for estimating local H-D allometries as well as mapping N and the mean quadratic diameter above 10 cm at the landscape level. Prior stratification into forest types is likely to improve both estimation procedures significantly and is considered the foremost current challenge.

One sixth of Amazonian tree diversity is dependent on river floodplains.

Amazonia's floodplain system is the largest and most biodiverse on Earth. Although forests are crucial to the ecological integrity of floodplains, our understanding of their species composition and how this may differ from surrounding forest types is still far too limited, particularly as changing inundation regimes begin to reshape floodplain tree communities and the critical ecosystem functions they underpin. Here we address this gap by taking a spatially explicit look at Amazonia-wide patterns of tree-species turnover and ecological specialization of the region's floodplain forests. We show that the majority of Amazonian tree species can inhabit floodplains, and about a sixth of Amazonian tree diversity is ecologically specialized on floodplains. The degree of specialization in floodplain communities is driven by regional flood patterns, with the most compositionally differentiated floodplain forests located centrally within the fluvial network and contingent on the most extraordinary flood magnitudes regionally. Our results provide a spatially explicit view of ecological specialization of floodplain forest communities and expose the need for whole-basin hydrological integrity to protect the Amazon's tree diversity and its function.

Mapping density, diversity and species-richness of the Amazon tree flora.

Using 2.046 botanically-inventoried tree plots across the largest tropical forest on Earth, we mapped tree species-diversity and tree species-richness at 0.1-degree resolution, and investigated drivers for diversity and richness. Using only location, stratified by forest type, as predictor, our spatial model, to the best of our knowledge, provides the most accurate map of tree diversity in Amazonia to date, explaining approximately 70% of the tree diversity and species-richness. Large soil-forest combinations determine a significant percentage of the variation in tree species-richness and tree alpha-diversity in Amazonian forest-plots. We suggest that the size and fragmentation of these systems drive their large-scale diversity patterns and hence local diversity. A model not using location but cumulative water deficit, tree density, and temperature seasonality explains 47% of the tree species-richness in the terra-firme forest in Amazonia. Over large areas across Amazonia, residuals of this relationship are small and poorly spatially structured, suggesting that much of the residual variation may be local. The Guyana Shield area has consistently negative residuals, showing that this area has lower tree species-richness than expected by our models. We provide extensive plot meta-data, including tree density, tree alpha-diversity and tree species-richness results and gridded maps at 0.1-degree resolution.

Unraveling Amazon tree community assembly using Maximum Information Entropy: a quantitative analysis of tropical forest ecology.

In a time of rapid global change, the question of what determines patterns in species abundance distribution remains a priority for understanding the complex dynamics of ecosystems. The constrained maximization of information entropy provides a framework for the understanding of such complex systems dynamics by a quantitative analysis of important constraints via predictions using least biased probability distributions. We apply it to over two thousand hectares of Amazonian tree inventories across seven forest types and thirteen functional traits, representing major global axes of plant strategies. Results show that constraints formed by regional relative abundances of genera explain eight times more of local relative abundances than constraints based on directional selection for specific functional traits, although the latter does show clear signals of environmental dependency. These results provide a quantitative insight by inference from large-scale data using cross-disciplinary methods, furthering our understanding of ecological dynamics.

Continental-scale patterns of canopy tree composition and function across Amazonia.

The world's greatest terrestrial stores of biodiversity and carbon are found in the forests of northern South America, where large-scale biogeographic patterns and processes have recently begun to be described. Seven of the nine countries with territory in the Amazon basin and the Guiana shield have carried out large-scale forest inventories, but such massive data sets have been little exploited by tropical plant ecologists. Although forest inventories often lack the species-level identifications favoured by tropical plant ecologists, their consistency of measurement and vast spatial coverage make them ideally suited for numerical analyses at large scales, and a valuable resource to describe the still poorly understood spatial variation of biomass, diversity, community composition and forest functioning across the South American tropics. Here we show, by using the seven forest inventories complemented with trait and inventory data collected elsewhere, two dominant gradients in tree composition and function across the Amazon, one paralleling a major gradient in soil fertility and the other paralleling a gradient in dry season length. The data set also indicates that the dominance of Fabaceae in the Guiana shield is not necessarily the result of root adaptations to poor soils (nodulation or ectomycorrhizal associations) but perhaps also the result of their remarkably high seed mass there as a potential adaptation to low rates of disturbance.

Relationships between species richness and ecosystem services in Amazonian forests strongly influenced by biogeographical strata and forest types.

Despite increasing attention for relationships between species richness and ecosystem services, for tropical forests such relationships are still under discussion. Contradicting relationships have been reported concerning carbon stock, while little is known about relationships concerning timber stock and the abundance of non-timber forest product producing plant species (NTFP abundance). Using 151 1-ha plots, we related tree and arborescent palm species richness to carbon stock, timber stock and NTFP abundance across the Guiana Shield, and using 283 1-ha plots, to carbon stock across all of Amazonia. We analysed how environmental heterogeneity influenced these relationships, assessing differences across and within multiple forest types, biogeographic regions and subregions. Species richness showed significant relationships with all three ecosystem services, but relationships differed between forest types and among biogeographical strata. We found that species richness was positively associated to carbon stock in all biogeographical strata. This association became obscured by variation across biogeographical regions at the scale of Amazonia, resembling a Simpson's paradox. By contrast, species richness was weakly or not significantly related to timber stock and NTFP abundance, suggesting that species richness is not a good predictor for these ecosystem services. Our findings illustrate the importance of environmental stratification in analysing biodiversity-ecosystem services relationships.

Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens.

Plant phenology is concerned with the timing of recurring biological events. Though phenology has traditionally been studied using intensive surveys of a local flora, results from such surveys are difficult to generalize to broader spatial scales. In this study, contrastingly, we assembled a continental-scale dataset of herbarium specimens for the emblematic genus of Neotropical pioneer trees, Cecropia, and applied Fourier spectral and cospectral analyses to investigate the reproductive phenology of 35 species. We detected significant annual, sub-annual and continuous patterns, and discuss the variation in patterns within and among climatic regions. Although previous studies have suggested that pioneer species generally produce flowers continually throughout the year, we found that at least one third of Cecropia species are characterized by clear annual flowering behaviour. We further investigated the relationships between phenology and climate seasonality, showing strong associations between phenology and seasonal variations in precipitation and temperature. We also verified our results against field survey data gathered from the literature. Our findings indicate that herbarium material is a reliable resource for use in the investigation of large-scale patterns in plant phenology, offering a promising complement to local intensive field studies.

Leaf functional response to increasing atmospheric CO(2) concentrations over the last century in two northern Amazonian tree species: a historical δ(13) C and δ(18) O approach using herbarium samples.

We assessed the extent of recent environmental changes on leaf morphological (stomatal density, stomatal surface, leaf mass per unit area) and physiological traits (carbon isotope composition, δ(13)C(leaf) , and discrimination, Δ(13)C(leaf) , oxygen isotope composition, δ(18)O(leaf) ) of two tropical rainforest species (Dicorynia guianensis; Humiria balsamifera) that are abundant in the Guiana shield (Northern Amazonia). Leaf samples were collected in different international herbariums to cover a 200 year time-period (1790-2004) and the whole Guiana shield. Using models describing carbon and oxygen isotope fractionations during photosynthesis, different scenarios of change in intercellular CO(2) concentrations inside the leaf (C(i)), stomatal conductance (g), and photosynthesis (A) were tested in order to understand leaf physiological response to increasing air CO(2) concentrations (C(a)). Our results confirmed that both species displayed physiological response to changing C(a) . For both species, we observed a decrease of about 1.7‰ in δ(13)C(leaf) since 1950, without significant change in Δ(13)C(leaf) and leaf morphological traits. Furthermore, there was no clear change in δ(18)O(leaf) for Humiria over this period. Our simulation approach revealed that an increase in A, rather than a decrease in g, explained the observed trends for these tropical rainforest species, allowing them to maintain a constant ratio of C(i)/C(a) .

Amazon tree dominance across forest strata.

The forests of Amazonia are among the most biodiverse plant communities on Earth. Given the immediate threats posed by climate and land-use change, an improved understanding of how this extraordinary biodiversity is spatially organized is urgently required to develop effective conservation strategies. Most Amazonian tree species are extremely rare but a few are common across the region. Indeed, just 227 'hyperdominant' species account for >50% of all individuals >10 cm diameter at 1.3 m in height. Yet, the degree to which the phenomenon of hyperdominance is sensitive to tree size, the extent to which the composition of dominant species changes with size class and how evolutionary history constrains tree hyperdominance, all remain unknown. Here, we use a large floristic dataset to show that, while hyperdominance is a universal phenomenon across forest strata, different species dominate the forest understory, midstory and canopy. We further find that, although species belonging to a range of phylogenetically dispersed lineages have become hyperdominant in small size classes, hyperdominants in large size classes are restricted to a few lineages. Our results demonstrate that it is essential to consider all forest strata to understand regional patterns of dominance and composition in Amazonia. More generally, through the lens of 654 hyperdominant species, we outline a tractable pathway for understanding the functioning of half of Amazonian forests across vertical strata and geographical locations.

Discrepancies between genetic and ecological divergence patterns suggest a complex biogeographic history in a Neotropical genus.

Phylogenetic patterns and the underlying speciation processes can be deduced from morphological, functional, and ecological patterns of species similarity and divergence. In some cases, though, species retain multiple similarities and remain almost indistinguishable; in other cases, evolutionary convergence can make such patterns misleading; very often in such cases, the "true" picture only emerges from carefully built molecular phylogenies, which may come with major surprises. In addition, closely related species may experience gene flow after divergence, thus potentially blurring species delimitation. By means of advanced inferential methods, we studied molecular divergence between species of the Virola genus (Myristicaceae): widespread Virola michelii and recently described, endemic V. kwatae, using widespread V. surinamensis as a more distantly related outgroup with different ecology and morphology-although with overlapping range. Contrary to expectations, we found that the latter, and not V. michelii, was sister to V. kwatae. Therefore, V. kwatae probably diverged from V. surinamensis through a recent morphological and ecological shift, which brought it close to distantly related V. michelii. Through the modeling of the divergence process, we inferred that gene flow between V. surinamensis and V. kwatae stopped soon after their divergence and resumed later, in a classical secondary contact event which did not erase their ecological and morphological differences. While we cannot exclude that initial divergence occurred in allopatry, current species distribution and the absence of geographical barriers make complete isolation during speciation unlikely. We tentatively conclude that (a) it is possible that divergence occurred in allopatry/parapatry and (b) secondary contact did not suppress divergence.

Biased-corrected richness estimates for the Amazonian tree flora.

Amazonian forests are extraordinarily diverse, but the estimated species richness is very much debated. Here, we apply an ensemble of parametric estimators and a novel technique that includes conspecific spatial aggregation to an extended database of forest plots with up-to-date taxonomy. We show that the species abundance distribution of Amazonia is best approximated by a logseries with aggregated individuals, where aggregation increases with rarity. By averaging several methods to estimate total richness, we confirm that over 15,000 tree species are expected to occur in Amazonia. We also show that using ten times the number of plots would result in an increase to just ~50% of those 15,000 estimated species. To get a more complete sample of all tree species, rigorous field campaigns may be needed but the number of trees in Amazonia will remain an estimate for years to come.

Towards a dynamic list of Amazonian tree species.

To provide an empirical foundation for estimates of the Amazonian tree diversity, we recently published a checklist of 11,675 tree species recorded to date in the region (ter Steege H, et al. (2016) The discovery of the Amazonian tree flora with an updated checklist of all known tree taxa. Scientific Reports 6:29549). From this total of plant records compiled from public databases and literature, widely used in studies on the Amazonian plant diversity, only 6,727 tree species belong to the first taxonomically-vetted checklist published for the region (Cardoso D, et al. (2017) Amazon plant diversity revealed by a taxonomically verified species list. PNAS 114:10695-10700). The striking difference in these two numbers spurred us to evaluate both lists, in order to release an improved Amazonian tree list; to discuss species inclusion criteria; and to highlight the ecological importance of verifying the occurrence of "non-Amazonian" trees in the region through the localization and identification of specimens. A number of species in the 2016 checklist that are not trees, non-native, synonyms, or misspellings were removed and corresponded to about 23% of the names. Species not included in the taxonomically-vetted checklist but verified by taxonomists to occur in Amazonia as trees were retained. Further, the inclusion of recently recorded/new species (after 2016), and recent taxonomic changes added up to an updated checklist including 10,071 species recorded for the Amazon region and shows the dynamic nature of establishing an authoritative checklist of Amazonian tree species. Completing and improving this list is a long-term, high-value commitment that will require a collaborative approach involving ecologists, taxonomists, and practitioners.

Chloroplast DNA variation in a hyperdiverse tropical tree community.

We investigate chloroplast DNA variation in a hyperdiverse community of tropical rainforest trees in French Guiana, focusing on patterns of intraspecific and interspecific variation. We test whether a species genetic diversity is higher when it has congeners in the community with which it can exchange genes and if shared haplotypes are more frequent in genetically diverse species, as expected in the presence of introgression.We sampled a total of 1,681 individual trees from 472 species corresponding to 198 genera and sequenced them at a noncoding chloroplast DNA fragment.Polymorphism was more frequent in species that have congeneric species in the study site than in those without congeners (30% vs. 12%). Moreover, more chloroplast haplotypes were shared with congeners in polymorphic species than in monomorphic ones (44% vs. 28%).Despite large heterogeneities caused by genus-specific behaviors in patterns of hybridization, these results suggest that the higher polymorphism in the presence of congeners is caused by local introgression rather than by incomplete lineage sorting. Our findings suggest that introgression has the potential to drive intraspecific genetic diversity in species-rich tropical forests.

Long-term influence of early human occupations on current forests of the Guiana Shield.

To decipher the long-term influences of pre-Columbian land occupations on contemporary forest structure, diversity, and functioning in Amazonia, most of the previous research focused on the alluvial plains of the major rivers of the Amazon basin. Terra firme, that is, nonflooded forests, particularly from the Guiana Shield, are yet to be explored. In this study, we aim to give new insights into the subtle traces of pre-Columbian influences on present-day forests given the archaeological context of terra firme forests of the Guiana Shield. Following archaeological prospects on 13 sites in French Guiana, we carried out forest inventories inside and outside archaeological sites and assessed the potential pre-Columbian use of the sampled tree species using an original ethnobotanical database of the Guiana Shield region. Aboveground biomass (320 and 380 T/ha, respectively), basal area (25-30 and 30-35 m2 /ha, respectively), and tree density (550 and 700 stem/ha, respectively) were all significantly lower on anthropized plots (As) than on nonanthropized plots (NAs). Ancient human presence shaped the species composition of the sampled forests with Arecaceae, Burseraceae, and Lauraceae significantly more frequent in As and Annonaceae and Lecythidaceae more frequent in NAs. Although alpha diversity was not different between As and NAs, the presence of pre-Columbian sites enhances significantly the forest beta diversity at the landscape level. Finally, trees with edible fruits are positively associated with pre-Columbian sites, whereas trees used for construction or for their bark are negatively associated with pre-Columbian sites. Half a millennium after their abandonment, former occupied places from the inner Guiana Shield still bear noticeable differences with nonanthropized places. Considering the lack of data concerning archaeology of terra firme Amazonian forests, our results suggest that pre-Columbian influences on the structure (lower current biomass), diversity (higher beta diversity), and composition (linked to the past human tree uses) of current Amazonian forests might be more important than previously thought.

Rarity of monodominance in hyperdiverse Amazonian forests.

Tropical forests are known for their high diversity. Yet, forest patches do occur in the tropics where a single tree species is dominant. Such "monodominant" forests are known from all of the main tropical regions. For Amazonia, we sampled the occurrence of monodominance in a massive, basin-wide database of forest-inventory plots from the Amazon Tree Diversity Network (ATDN). Utilizing a simple defining metric of at least half of the trees ≥ 10 cm diameter belonging to one species, we found only a few occurrences of monodominance in Amazonia, and the phenomenon was not significantly linked to previously hypothesized life history traits such wood density, seed mass, ectomycorrhizal associations, or Rhizobium nodulation. In our analysis, coppicing (the formation of sprouts at the base of the tree or on roots) was the only trait significantly linked to monodominance. While at specific locales coppicing or ectomycorrhizal associations may confer a considerable advantage to a tree species and lead to its monodominance, very few species have these traits. Mining of the ATDN dataset suggests that monodominance is quite rare in Amazonia, and may be linked primarily to edaphic factors.