Understanding different dominance patterns in western Amazonian forests.

Dominance of neotropical tree communities by a few species is widely documented, but dominant trees show a variety of distributional patterns still poorly understood. Here, we used 503 forest inventory plots (93,719 individuals ≥2.5 cm diameter, 2609 species) to explore the relationships between local abundance, regional frequency and spatial aggregation of dominant species in four main habitat types in western Amazonia. Although the abundance-occupancy relationship is positive for the full dataset, we found that among dominant Amazonian tree species, there is a strong negative relationship between local abundance and regional frequency and/or spatial aggregation across habitat types. Our findings suggest an ecological trade-off whereby dominant species can be locally abundant (local dominants) or regionally widespread (widespread dominants), but rarely both (oligarchs). Given the importance of dominant species as drivers of diversity and ecosystem functioning, unravelling different dominance patterns is a research priority to direct conservation efforts in Amazonian forests.

Niche breadth of Amazonian trees increases with niche optimum across broad edaphic gradients.

Understanding how biotic interactions and environmental filtering mediated by soil properties shape plant community assembly is a major challenge in ecology, especially when studying complex and hyperdiverse ecosystems like tropical forests. To shed light on the influence of both factors, we examined how the edaphic optimum of species (their niche position) related to their edaphic range (their niche breadth) along different environmental gradients and how this translates into functional strategies. Here we tested four scenarios describing the shape of the niche breadth-niche position relationship, including one neutral scenario and three scenarios proposing different relative influences of abiotic and biotic factors on community assembly along a soil resource gradient. To do so, we used soil concentration data for five key nutrients (N, P, Ca, Mg, and K), along with accurate measurements of 14 leaf, stem, and root traits for 246 tree species inventoried in 101 plots located across Eastern (French Guiana) and Western (Peru) Amazonia. We found that species niche breadth increased linearly with species niche position along each soil nutrient gradient. This increase was associated with more resource acquisitive traits in the leaves and the roots for soil N, Ca, Mg, and K concentration, while it was negatively associated with wood density for soil P concentration. These observations agreed with one of our hypothetical scenarios in which species with resource conservation traits are confined to the most nutrient-depleted soils (abiotic filter), but they are outperformed by faster-growing species in more fertile conditions (biotic filter). Our results refine and strengthen support for niche theories of species assembly while providing an integrated approach to improving forest management policies.

Parallel evolution and cryptic diversification in a common and widespread Amazonian tree, Protium subserratum.

The lowland Amazon rainforest houses some of the greatest tree diversity on Earth. While the vast majority of these species are rare, a small number are common and widespread and thus considered to play a disproportionate role in many of the global ecosystem services provided by the Amazon. However, the extent to which dominant Amazonian tree species actually include multiple clades, each on their own unique evolutionary trajectory, is unknown. Here we investigate the extent to which lineage divergence may be occurring within Protium subserratum (Burseraceae), a common and widespread tree species that is monophyletic with populations exhibiting genotypic and phenotypic differences associated with soil and geography. Utilizing a combination of phylogenomic and population genomic methods with sampling from across the range, we found that P. subserratum contains at least eight distinct clades. Specialization onto white-sand soils has evolved independently at least twice within the species; however, phenotype is not correlated with soil type. Finally, cryptic diversity at the base of the Andes is associated with elevational shifts. Together these results lend support to the hypothesis that common and widespread Amazon tree species may not represent evolutionary cohesive units. Instead, these dominant species may more commonly represent species complexes, undergoing evolutionary transitions on a trajectory to become multiple range-restricted, specialist species.

A nuclear target sequence capture probe set for phylogeny reconstruction of the charismatic plant family Bignoniaceae.

The plant family Bignoniaceae is a conspicuous and charismatic element of the tropical flora. The family has a complex taxonomic history, with substantial changes in the classification of the group during the past two centuries. Recent re-classifications at the tribal and generic levels have been largely possible by the availability of molecular phylogenies reconstructed using Sanger sequencing data. However, our complete understanding of the systematics, evolution, and biogeography of the family remains incomplete, especially due to the low resolution and support of different portions of the Bignoniaceae phylogeny. To overcome these limitations and increase the amount of molecular data available for phylogeny reconstruction within this plant family, we developed a bait kit targeting 762 nuclear genes, including 329 genes selected specifically for the Bignoniaceae; 348 genes obtained from the Angiosperms353 with baits designed specifically for the family; and, 85 low-copy genes of known function. On average, 77.4% of the reads mapped to the targets, and 755 genes were obtained per species. After removing genes with putative paralogs, 677 loci were used for phylogenetic analyses. On-target genes were compared and combined in the Exon-Only dataset, and on-target + off-target regions were combined in the Supercontig dataset. We tested the performance of the bait kit at different taxonomic levels, from family to species-level, using 38 specimens of 36 different species of Bignoniaceae, representing: 1) six (out of eight) tribal level-clades (e.g., Bignonieae, Oroxyleae, Tabebuia Alliance, Paleotropical Clade, Tecomeae, and Jacarandeae), only Tourrettieae and Catalpeae were not sampled; 2) all 20 genera of Bignonieae; 3) seven (out of nine) species of Dolichandra (e.g., D. chodatii, D. cynanchoides, D. dentata, D. hispida, D. quadrivalvis, D. uncata, and D. uniguis-cati), only D. steyermarkii and D. unguiculata were not sampled; and 4) three individuals of Dolichandra unguis-cati. Our data reconstructed a well-supported phylogeny of the Bignoniaceae at different taxonomic scales, opening new perspectives for a comprehensive phylogenetic framework for the family as a whole.

The contribution of environmental and dispersal filters on phylogenetic and taxonomic beta diversity patterns in Amazonian tree communities.

Environmental and dispersal filters are key determinants of species distributions of Amazonian tree communities. However, a comprehensive analysis of the role of environmental and dispersal filters is needed to understand the ecological and evolutionary processes that drive phylogenetic and taxonomic turnover of Amazonian tree communities. We compare measures of taxonomic and phylogenetic beta diversity in 41 one-hectare plots to test the relative importance of climate, soils, geology, geomorphology, pure spatial variables and the spatial variation of environmental drivers of phylogenetic and taxonomic turnover in Ecuadorian Amazon tree communities. We found low phylogenetic and high taxonomic turnover with respect to environmental and dispersal filters. In addition, our results suggest that climate is a significantly better predictor of phylogenetic turnover and taxonomic turnover than geomorphology and soils at all spatial scales. The influence of climate as a predictor of phylogenetic turnover was stronger at broader spatial scales (50 km2) whereas geomorphology and soils appear to be better predictors of taxonomic turnover at mid (5 km2) and fine spatial scales (0.5 km2) but a weak predictor of phylogenetic turnover at broad spatial scales. We also found that the combined effect of geomorphology and soils was significantly higher for taxonomic turnover at all spatial scales but not for phylogenetic turnover at large spatial scales. Geographic distances as proxy of dispersal limitation was a better predictor of phylogenetic turnover at distances of 50 < 500 km. Our findings suggest that climatic variation at regional scales can better predict phylogenetic and taxonomic turnover than geomorphology and soils.

Revisiting the hyperdominance of Neotropical tree species under a taxonomic, functional and evolutionary perspective.

Recent studies have leveraged large datasets from plot-inventory networks to report a phenomenon of hyperdominance in Amazonian tree communities, concluding that few species are common and many are rare. However, taxonomic hypotheses may not be consistent across these large plot networks, potentially masking cryptic diversity and threatened rare taxa. In the current study, we have reviewed one of the most abundant putatively hyperdominant taxa, Protium heptaphyllum (Aubl.) Marchand (Burseraceae), long considered to be a taxonomically difficult species complex. Using morphological, genomic, and functional data, we present evidence that P. heptaphyllum sensu lato may represent eight separately evolving lineages, each warranting species status. Most of these lineages are geographically restricted, and few if any of them could be considered hyperdominant on their own. In addition, functional trait data are consistent with the hypothesis that trees from each lineage are adapted to distinct soil and climate conditions. Moreover, some of the newly discovered species are rare, with habitats currently experiencing rapid deforestation. We highlight an urgent need to improve sampling and methods for species discovery in order to avoid oversimplified assumptions regarding diversity and rarity in the tropics and the implications for ecosystem functioning and conservation.

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.

Genomic and phenotypic divergence unveil microgeographic adaptation in the Amazonian hyperdominant tree Eperua falcata Aubl. (Fabaceae).

Plant populations can undergo very localized adaptation, allowing widely distributed populations to adapt to divergent habitats in spite of recurrent gene flow. Neotropical trees-whose large and undisturbed populations often span a variety of environmental conditions and local habitats-are particularly good models to study this process. Here, we explore patterns of adaptive divergence from large (i.e., regional) to small (i.e., microgeographic) spatial scales in the hyperdominant Amazonian tree Eperua falcata Aubl. (Fabaceae) under a replicated design involving two microhabitats (~300 m apart) in two study sites (~300 km apart). A three-year reciprocal transplant illustrates that, beyond strong maternal effects and phenotypic plasticity, genetically driven divergence in seedling growth and leaf traits was detected both between seedlings originating from different regions, and between seedlings from different microhabitats. In parallel, a complementary genome scan for selection was carried out through whole-genome sequencing of tree population pools. A set of 290 divergence outlier SNPs was detected at the regional scale (between study sites), while 185 SNPs located in the vicinity of 106 protein-coding genes were detected as replicated outliers between microhabitats within regions. Outlier-surrounding genomic regions are involved in a variety of physiological processes, including plant responses to stress (e.g., oxidative stress, hypoxia and metal toxicity) and biotic interactions. Together with evidence of microgeographic divergence in functional traits, the discovery of genomic candidates for microgeographic adaptive divergence represents a promising advance in our understanding of local adaptation, which probably operates across multiple spatial scales and underpins divergence and diversification in Neotropical trees.

Natural selection maintains species despite frequent hybridization in the desert shrub Encelia.

Natural selection is an important driver of genetic and phenotypic differentiation between species. For species in which potential gene flow is high but realized gene flow is low, adaptation via natural selection may be a particularly important force maintaining species. For a recent radiation of New World desert shrubs (Encelia: Asteraceae), we use fine-scale geographic sampling and population genomics to determine patterns of gene flow across two hybrid zones formed between two independent pairs of species with parapatric distributions. After finding evidence for extremely strong selection at both hybrid zones, we use a combination of field experiments, high-resolution imaging, and physiological measurements to determine the ecological basis for selection at one of the hybrid zones. Our results identify multiple ecological mechanisms of selection (drought, salinity, herbivory, and burial) that together are sufficient to maintain species boundaries despite high rates of hybridization. Given that multiple pairs of Encelia species hybridize at ecologically divergent parapatric boundaries, such mechanisms may maintain species boundaries throughout Encelia.

The contribution of multiple barriers to reproduction between edaphically divergent lineages in the Amazonian tree Protium subserratum (Burseraceae).

Disentangling the strength and importance of barriers to reproduction that arise between diverging lineages is central to our understanding of species origin and maintenance. To date, the vast majority of studies investigating the importance of different barriers to reproduction in plants have focused on short-lived temperate taxa while studies of reproductive isolation in trees and tropical taxa are rare. Here, we systematically examine multiple barriers to reproduction in an Amazonian tree, Protium subserratum (Burseraceae) with diverging lineages of soil specialist ecotypes. Using observational, molecular, distributional, and experimental data, we aimed to quantify the contributions of individual prezygotic and postzygotic barriers including ecogeographic isolation, flowering phenology, pollinator assemblage, pollen adhesion, pollen germination, pollen tube growth, seed development, and hybrid fitness to total reproductive isolation between the ecotypes. We were able to identify five potential barriers to reproduction including ecogeographic isolation, phenological differences, differences in pollinator assemblages, differential pollen adhesion, and low levels of hybrid seed development. We demonstrate that ecogeographic isolation is a strong and that a combination of intrinsic and extrinsic prezygotic and postzygotic barriers may be acting to maintain near complete reproductive isolation between edaphically divergent populations of the tropical tree, P. subserratum.

Convergent evolution of tree hydraulic traits in Amazonian habitats: implications for community assemblage and vulnerability to drought.

Amazonian droughts are increasing in frequency and severity. However, little is known about how this may influence species-specific vulnerability to drought across different ecosystem types. We measured 16 functional traits for 16 congeneric species from six families and eight genera restricted to floodplain, swamp, white-sand or plateau forests of Central Amazonia. We investigated whether habitat distributions can be explained by species hydraulic strategies, and if habitat specialists differ in their vulnerability to embolism that would make water transport difficult during drought periods. We found strong functional differences among species. Nonflooded species had higher wood specific gravity and lower stomatal density, whereas flooded species had wider vessels, and higher leaf and xylem hydraulic conductivity. The P50 values (water potential at 50% loss of hydraulic conductivity) of nonflooded species were significantly more negative than flooded species. However, we found no differences in hydraulic safety margin among species, suggesting that all trees may be equally likely to experience hydraulic failure during severe droughts. Water availability imposes a strong selection leading to differentiation of plant hydraulic strategies among species and may underlie patterns of adaptive radiation in many tropical tree genera. Our results have important implications for modeling species distribution and resilience under future climate scenarios.

Sesenta y cuatro nuevos registros para la flora del Perú a través de inventarios biológicos rápidos en la Amazonía peruana

Durante el período 2000 - 2016, se llevaron a cabo 15 inventarios biológicos en áreas remotas en el pie de monte andino y el llano amazónico del Perú. En estos inventarios, 27 botánicos colectaron un total de 9397 especímenes de plantas vasculares fértiles. Hasta finales del 2017, más de la mitad de estos especímenes se han identificado a nivel de especie, de los cuales 64 especies y 2 géneros (Dicorynia y Monopteryx) representan nuevos registros para la flora del Perú. Si esta tasa de novedades se mantiene, el número de registros nuevos en el material de los inventarios podría aumentar, lo cual nos indica que aún queda mucho por descubrir en la flora andino-amazónica del Perú.

Between 2000 and 2016 we carried out 15 rapid biological inventories in remote areas of the Andean foothills and Amazon basin in Peru. During these inventories, 27 botanists collected 9397 fertile vascular plant specimens. By the end of 2017, more than half of these specimens had been identified to species. Of the 2303 species identified to date, 64 species and 2 genera (Dicorynia and Monopteryx) are new records for the flora of Peru. If this rate of discovery proves typical, the number of new records for Peru in the rapid inventory material could increase, which indicates that there is still much to discover in the Peruvian flora.

Leaf Transcriptome Assembly of Protium copal (Burseraceae) and Annotation of Terpene Biosynthetic Genes.

Plants in the Burseraceae are globally recognized for producing resins and essential oils with medicinal properties and have economic value. In addition, most of the aromatic and non-aromatic components of Burseraceae resins are derived from a variety of terpene and terpenoid chemicals. Although terpene genes have been identified in model plant crops (e.g., Citrus, Arabidopsis), very few genomic resources are available for non-model groups, including the highly diverse Burseraceae family. Here we report the assembly of a leaf transcriptome of Protium copal, an aromatic tree that has a large distribution in Central America, describe the functional annotation of putative terpene biosynthetic genes and compare terpene biosynthetic genes found in P. copal with those identified in other Burseraceae taxa. The genomic resources of Protium copal can be used to generate novel sequencing markers for population genetics and comparative phylogenetic studies, and to investigate the diversity and evolution of terpene genes in the Burseraceae.

Dominant tree species drive beta diversity patterns in western Amazonia.

The forests of western Amazonia are among the most diverse tree communities on Earth, yet this exceptional diversity is distributed highly unevenly within and among communities. In particular, a small number of dominant species account for the majority of individuals, whereas the large majority of species are locally and regionally extremely scarce. By definition, dominant species contribute little to local species richness (alpha diversity), yet the importance of dominant species in structuring patterns of spatial floristic turnover (beta diversity) has not been investigated. Here, using a network of 207 forest inventory plots, we explore the role of dominant species in determining regional patterns of beta diversity (community-level floristic turnover and distance-decay relationships) across a range of habitat types in northern lowland Peru. Of the 2,031 recorded species in our data set, only 99 of them accounted for 50% of individuals. Using these 99 species, it was possible to reconstruct the overall features of regional beta diversity patterns, including the location and dispersion of habitat types in multivariate space, and distance-decay relationships. In fact, our analysis demonstrated that regional patterns of beta diversity were better maintained by the 99 dominant species than by the 1,932 others, whether quantified using species-abundance data or species presence-absence data. Our results reveal that dominant species are normally common only in a single forest type. Therefore, dominant species play a key role in structuring western Amazonian tree communities, which in turn has important implications, both practically for designing effective protected areas, and more generally for understanding the determinants of beta diversity patterns.

Dry and hot: the hydraulic consequences of a climate change-type drought for Amazonian trees.

How plants respond physiologically to leaf warming and low water availability may determine how they will perform under future climate change. In 2015-2016, an unprecedented drought occurred across Amazonia with record-breaking high temperatures and low soil moisture, offering a unique opportunity to evaluate the performances of Amazonian trees to a severe climatic event. We quantified the responses of leaf water potential, sap velocity, whole-tree hydraulic conductance (Kwt), turgor loss and xylem embolism, during and after the 2015-2016 El Niño for five canopy-tree species. Leaf/xylem safety margins (SMs), sap velocity and Kwt showed a sharp drop during warm periods. SMs were negatively correlated with vapour pressure deficit, but had no significant relationship with soil water storage. Based on our calculations of canopy stomatal and xylem resistances, the decrease in sap velocity and Kwt was due to a combination of xylem cavitation and stomatal closure. Our results suggest that warm droughts greatly amplify the degree of trees' physiological stress and can lead to mortality. Given the extreme nature of the 2015-2016 El Niño and that temperatures are predicted to increase, this work can serve as a case study of the possible impact climate warming can have on tropical trees.This article is part of a discussion meeting issue 'The impact of the 2015/2016 El Niño on the terrestrial tropical carbon cycle: patterns, mechanisms and implications'.

Divergent Secondary Metabolites and Habitat Filtering Both Contribute to Tree Species Coexistence in the Peruvian Amazon.

Little is known about the mechanisms promoting or limiting the coexistence of functionally divergent species in hyperdiverse tropical tree genera. Density-dependent enemy attacks have been proposed to be a major driver for the local coexistence of chemically divergent congeneric species. At the same time, we expect local soil conditions to favor the coexistence of species sharing similar functional traits related to resource use strategies, while environmental heterogeneity would promote the diversity of these traits at both local and large spatial scales. To test how these traits mediate species coexistence, we used functional trait data for 29 species from the tree genus Protium (Burseraceae), collected in 19 plots (2 ha each) in the Peruvian Amazon. We characterized the presence-absence of 189 plant secondary metabolites (SM) for 27 of these species, and 14 functional traits associated with resource use strategies (RUT) for 16 species. Based on these data, we found that SM were significantly more dissimilar than null expectations for species co-occurring within plots, whereas RUT were significantly more similar. These results were consistent with the hypothesis that density-dependent enemy attacks contribute to the local coexistence of congeneric species displaying divergent chemical defenses, whereas local habitat conditions filter species with similar RUT. Using measurements of nine soil properties in each plot, we also found a significant turnover of RUT traits with increasing dissimilarity of soil texture and nutrient availabilities, providing support for the hypothesis that soil heterogeneity maintains functional diversity at larger spatial scales (from 500 m up to ca. 200 km) in Protium communities. Our study provides new evidence suggesting that density-dependent enemy attacks and soil heterogeneity both contribute to maintaining high species richness in diverse tropical forests.

Origin and maintenance of chemical diversity in a species-rich tropical tree lineage.

Plant secondary metabolites play important ecological and evolutionary roles, most notably in the deterrence of natural enemies. The classical theory explaining the evolution of plant chemical diversity is that new defences arise through a pairwise co-evolutionary arms race between plants and their specialized natural enemies. However, plant species are bombarded by dozens of different herbivore taxa from disparate phylogenetic lineages that span a wide range of feeding strategies and have distinctive physiological constraints that interact differently with particular plant metabolites. How do plant defence chemicals evolve under such multiple and potentially contrasting selective pressures imposed by diverse herbivore communities? To tackle this question, we exhaustively characterized the chemical diversity and insect herbivore fauna from 31 sympatric species of Amazonian Protieae (Burseraceae) trees. Using a combination of phylogenetic, metabolomic and statistical learning tools, we show that secondary metabolites that were associated with repelling herbivores (1) were more frequent across the Protieae phylogeny and (2) were found in average higher abundance than other compounds. Our findings suggest that generalist herbivores can play an important role in shaping plant chemical diversity and support the hypothesis that chemical diversity can also arise from the cumulative outcome of multiple diffuse interactions.

Incorporating phylogenetic information for the definition of floristic districts in hyperdiverse Amazon forests: Implications for conservation.

Using complementary metrics to evaluate phylogenetic diversity can facilitate the delimitation of floristic units and conservation priority areas. In this study, we describe the spatial patterns of phylogenetic alpha and beta diversity, phylogenetic endemism, and evolutionary distinctiveness of the hyperdiverse Ecuador Amazon forests and define priority areas for conservation. We established a network of 62 one-hectare plots in terra firme forests of Ecuadorian Amazon. In these plots, we tagged, collected, and identified every single adult tree with dbh ≥10 cm. These data were combined with a regional community phylogenetic tree to calculate different phylogenetic diversity (PD) metrics in order to create spatial models. We used Loess regression to estimate the spatial variation of taxonomic and phylogenetic beta diversity as well as phylogenetic endemism and evolutionary distinctiveness. We found evidence for the definition of three floristic districts in the Ecuadorian Amazon, supported by both taxonomic and phylogenetic diversity data. Areas with high levels of phylogenetic endemism and evolutionary distinctiveness in Ecuadorian Amazon forests are unprotected. Furthermore, these areas are severely threatened by proposed plans of oil and mining extraction at large scales and should be prioritized in conservation planning for this region.