Amazonian White-Sand Forests Show Strong Floristic Links with Surrounding Oligotrophic Habitats and the Guiana Shield

Recognizing and understanding historical patterns and processes that have influenced the diversification of organisms on earth is one of the central goals of evolutionary biology. Within this broad area, studies within the disciplines of molecular systematics (i.e. phylogeography, phylogenetics and population genetics), allow us to address evolutionary questions from different biological, spatial and temporal scales. Phylogeography and molecular phylogenetics help us to understand aspects related to events that have given rise to patterns of genetic variation in organisms, as well as to understand the assembly of biological communities in a given area. These types of studies provide crucial information to increase knowledge about the biodiversity of little-studied ecoregions. One such ecoregion is Colombian Guyana. This ecoregion, which is located between three putative centers of speciation; Amazonia, the Andes and Guyana, is one of the least explored areas of the country. As a result of their geological composition, the western enclaves of the Guiana Shield have been described as a "heterogeneous entity", composed of savannas, catingas, lowland forests, and even white sand forests. Using bats as a biological study group, this paper presents two approaches focused on understanding how biogeographic events that have shaped the diversity of the continent have affected different lineages that inhabit Colombian Guiana. Bats are a group of vertebrates sensitive to biogeographic events that have shaped the diversity of the continent, which play different functional roles in the ecosystems they inhabit. High degrees of association with habitat have been described for numerous bat species, mainly in terms of foraging characteristics and diet types. In a first project, we comparatively analyzed the phylogeographic patterns of three widely distributed bat species, with the aim of identifying the patterns of genetic divergence of the bats that inhabit the area today. Using mitochondrial DNA sequences, we revealed the existence of bat populations established in the area, which showed different degrees of gene flow with surrounding biogeographic areas, especially with the Guiana provinces of Oriente and Pantepui and the Amazon. Additionally, we identified different demographic histories for each species, which were probably influenced to different extents by climatic changes during the Pleistocene and differential ecological characteristics. Our results highlight the influence of Colombian Guiana ecosystems on the formation and spatial configuration of bat diversity and genetic structure, and the importance of these ecosystems for bat conservation. In a second project, from a phylogenetic perspective, we evaluated the phylogenetic structure of bat communities inhabiting different eco-regions of northern South America, using mitochondrial and nuclear DNA sequences. The results of the analysis allowed us to demonstrate that the bat populations of the Western Guayana Province (which includes the Colombian portion of the Guiana Shield), are phylogenetically clustered, that is, the species that compose the communities are evolutionarily closer than expected by chance. We conclude that factors such as the high heterogeneity of habitats in the region, the high diversity of fruit bats in the sampled communities, and interspecific competition have shaped the species composition of the communities in this area. In a final chapter, a general discussion of the results obtained from the two research projects carried out is developed. Chapters one and two of this thesis will be submitted to international indexed journals, which is why they are written in English and in scientific article format.Reconocer y entender patrones y procesos históricos que han influenciado la diversificación de los organismos sobre la tierra, es uno de los objetivos centrales de la biología evolutiva. Dentro de esta gran área, estudios enmarcados en las disciplinas de la sistemática molecular (i.e. filogeografía, filogenética y genética de poblaciones), nos permiten abordar preguntas evolutivas desde diferentes escalas biológicas, espaciales y temporales. La filogeografía y la filogenética molecular nos ayudan a entender aspectos relacionados con eventos que han dado lugar a patrones de variación genética de los organismos, así como entender el ensamblaje de comunidades biológicas en un área determinada. Este tipo de estudios aportan información crucial para aumentar el conocimiento acerca de biodiversidad de eco regiones poco estudiadas. Una de estas eco regiones es la Guyana colombiana. Esta eco región, la cual se encuentra ubicada entre tres centros putativos de especiación; Amazonía, Andes y Guayana, es una de las zonas menos exploradas del país. Como resultado de su composición geológica, los enclaves occidentales del escudo Guayanés han sido descritos como una "entidad heterogénea", compuesta de sabanas, catingas, bosques bajos, e inclusive bosques de arena blanca. Usando como grupo biológico de estudio los murciélagos, este trabajo de grado presentan dos aproximaciones enfocadas a entender como eventos biogeográficos que han moldeado la diversidad del continente, han afectado diferentes linajes que habitan la Guayana colombiana. Los murciélagos son un grupo de vertebrados sensibles a los eventos biogeográficos que han moldeado la diversidad del continente, el cuál cumple diferentes roles funcionales en los ecosistemas que habitan. Altos grados de asociación con el hábitat han sido descritos para numerosas especies de murciélagos, principalmente en cuanto a características de forrajeo y tipos de dieta. En un primer proyecto, analizamos comparativamente los patrones filogeográficos de tres especies de murciélagos de amplia distribución, con el objetivo de identificar los patrones de divergencia genética de los murciélagos que habitan el área en la actualidad. Utilizando secuencias de ADN mitocondrial, revelamos la existencia de poblaciones de murciélagos establecidas en el área, las cuales mostraron diferentes grados de flujo genético con áreas biogeográficas circundantes, en especial con las provincias guayanesas del Oriente y Pantepui y el Amazonas. Adicionalmente identificamos diferentes historias demográficas para cada especie, las cuales probablemente fueron influenciadas en diferente medida por cambios climáticos durante el pleistoceno y características ecológicas diferenciales. Nuestros resultados destacan la influencia de los ecosistemas guayaneses colombianos en la formación y configuración espacial de la diversidad y estructura genética en murciélagos, y la importancia de estos ecosistemas para la conservación dicha diversidad. En un segundo proyecto, desde una perspectiva filogenética, evaluamos la estructura filogenética de la comunidad de murciélagos de diferentes eco-regiones del norte de sur américa, usando secuencia de ADN mitocondrial. Los resultados de los análisis nos permitieron demostrar que las poblaciones de murciélagos de la Provincia Guayanesa del Occidente (la cual incluye la porción colombiana del escudo guayanés), se encuentran filogenéticamente agregadas, es decir, las especies que componen las comunidades son más cercanas evolutivamente de lo esperado por el azar. Concluimos que factores como la alta heterogeneidad de hábitats en la región, la alta diversidad de murciélagos frugívoros en las comunidades muestreadas, y la competencia interespecífica han moldeado la composición de especies de las comunidades en esta zona. En un capítulo final, se desarrolla una discusión general de los resultados obtenidos de los dos proyectos de investigación realizados. Los capítulos uno y dos de esta tesis serán sometidos a revistas indexadas internacionales, razón por la cual están escritos en idioma inglés y en formato de artículo científico.Línea de Investigación: Biología EvolutivaMaestrí

Palm species richness, latitudinal gradients, sampling effort, and deforestation in the Amazon region

Palms are most diverse in warm and humid regions near the equator. Though palms remain relatively well conserved, they are under increasing pressure from deforestation. Here, we analyze patterns of palm species richness relative to latitudinal gradient, sampling effort, and deforestation in the Amazon, and compare patterns of richness and floristic similarity among Amazonian sub-regions. We built a database of 17,310 records for 177 species. The areas with the greatest richness were in the western, central and northeastern Amazon, principally at latitudes 0-5ºS. Species richness and the number of records were highly correlated (R2=0.76, P2000 km2) were found in the southern and eastern Amazon of Brazil, which coincide with low richness and gaps in records. Similarity analyzes resulted in two groups of sub-regions: the first included the Amazon s.s., the Andes and the Guiana, while the second included the Plateau and Gurupi. We conclude that the highest species richness is at low latitudes, and observed richness is affected by sampling effort and is vulnerable to deforestation. Therefore, areas with low species richness, especially areas with data deficiency, need to be further studied for a better understanding of their patterns of diversity and richness.

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

Geographic patterns of tree dispersal modes in Amazonia and their ecological correlates

Unidad de excelencia María de Maeztu CEX2019-000940-MAim: To investigate the geographic patterns and ecological correlates in the geographic distribution of the most common tree dispersal modes in Amazonia (endozoochory, synzoochory, anemochory and hydrochory). We examined if the proportional abundance of these dispersal modes could be explained by the availability of dispersal agents (disperser-availability hypothesis) and/or the availability of resources for constructing zoochorous fruits (resource-availability hypothesis). Time period: Tree-inventory plots established between 1934 and 2019. Major taxa studied: Trees with a diameter at breast height (DBH) ≥ 9.55 cm. Location: Amazonia, here defined as the lowland rain forests of the Amazon River basin and the Guiana Shield. Methods: We assigned dispersal modes to a total of 5433 species and morphospecies within 1877 tree-inventory plots across terra-firme, seasonally flooded, and permanently flooded forests. We investigated geographic patterns in the proportional abundance of dispersal modes. We performed an abundance-weighted mean pairwise distance (MPD) test and fit generalized linear models (GLMs) to explain the geographic distribution of dispersal modes. Results: Anemochory was significantly, positively associated with mean annual wind speed, and hydrochory was significantly higher in flooded forests. Dispersal modes did not consistently show significant associations with the availability of resources for constructing zoochorous fruits. A lower dissimilarity in dispersal modes, resulting from a higher dominance of endozoochory, occurred in terra-firme forests (excluding podzols) compared to flooded forests. Main conclusions: The disperser-availability hypothesis was well supported for abiotic dispersal modes (anemochory and hydrochory). The availability of resources for constructing zoochorous fruits seems an unlikely explanation for the distribution of dispersal modes in Amazonia. The association between frugivores and the proportional abundance of zoochory requires further research, as tree recruitment not only depends on dispersal vectors but also on conditions that favour or limit seedling recruitment across forest types

Estimating the global conservation status of more than 15,000 Amazonian tree species

Estimates of extinction risk for Amazonian plant and animal species are rare and not often incorporated into land-use policy and conservation planning. We overlay spatial distribution models with historical and projected deforestation to show that at least 36% and up to 57% of all Amazonian tree species are likely to qualify as globally threatened under International Union for Conservation of Nature (IUCN) Red List criteria. If confirmed, these results would increase the number of threatened plant species on Earth by 22%. We show that the trends observed in Amazonia apply to trees throughout the tropics, and we predict thatmost of the world’s >40,000 tropical tree species now qualify as globally threatened. A gap analysis suggests that existing Amazonian protected areas and indigenous territories will protect viable populations of most threatened species if these areas suffer no further degradation, highlighting the key roles that protected areas, indigenous peoples, and improved governance can play in preventing large-scale extinctions in the tropics in this century

Local hydrological conditions influence tree diversity and composition across the Amazon basin

Tree diversity and composition in Amazonia are known to be strongly determined by the water supplied by precipitation. Nevertheless, within the same climatic regime, water availability is modulated by local topography and soil characteristics (hereafter referred to as local hydrological conditions), varying from saturated and poorly drained to well-drained and potentially dry areas. While these conditions may be expected to influence species distribution, the impacts of local hydrological conditions on tree diversity and composition remain poorly understood at the whole Amazon basin scale. Using a dataset of 443 1-ha non-flooded forest plots distributed across the basin, we investigate how local hydrological conditions influence 1) tree alpha diversity, 2) the community-weighted wood density mean (CWM-wd) – a proxy for hydraulic resistance and 3) tree species composition. We find that the effect of local hydrological conditions on tree diversity depends on climate, being more evident in wetter forests, where diversity increases towards locations with well-drained soils. CWM-wd increased towards better drained soils in Southern and Western Amazonia. Tree species composition changed along local soil hydrological gradients in Central-Eastern, Western and Southern Amazonia, and those changes were correlated with changes in the mean wood density of plots. Our results suggest that local hydrological gradients filter species, influencing the diversity and composition of Amazonian forests. Overall, this study shows that the effect of local hydrological conditions is pervasive, extending over wide Amazonian regions, and reinforces the importance of accounting for local topography and hydrology to better understand the likely response and resilience of forests to increased frequency of extreme climate events and rising temperatures

Geographic patterns of tree dispersal modes in Amazonia and their ecological correlates

Aim: To investigate the geographic patterns and ecological correlates in the geographic distribution of the most common tree dispersal modes in Amazonia (endozoochory, synzoochory, anemochory and hydrochory). We examined if the proportional abundance of these dispersal modes could be explained by the availability of dispersal agents (disperser-availability hypothesis) and/or the availability of resources for constructing zoochorous fruits (resource-availability hypothesis). Time period: Tree-inventory plots established between 1934 and 2019. Major taxa studied: Trees with a diameter at breast height (DBH) ≥ 9.55 cm. Location: Amazonia, here defined as the lowland rain forests of the Amazon River basin and the Guiana Shield. Methods: We assigned dispersal modes to a total of 5433 species and morphospecies within 1877 tree-inventory plots across terra-firme, seasonally flooded, and permanently flooded forests. We investigated geographic patterns in the proportional abundance of dispersal modes. We performed an abundance-weighted mean pairwise distance (MPD) test and fit generalized linear models (GLMs) to explain the geographic distribution of dispersal modes. Results: Anemochory was significantly, positively associated with mean annual wind speed, and hydrochory was significantly higher in flooded forests. Dispersal modes did not consistently show significant associations with the availability of resources for constructing zoochorous fruits. A lower dissimilarity in dispersal modes, resulting from a higher dominance of endozoochory, occurred in terra-firme forests (excluding podzols) compared to flooded forests. Main conclusions: The disperser-availability hypothesis was well supported for abiotic dispersal modes (anemochory and hydrochory). The availability of resources for constructing zoochorous fruits seems an unlikely explanation for the distribution of dispersal modes in Amazonia. The association between frugivores and the proportional abundance of zoochory requires further research, as tree recruitment not only depends on dispersal vectors but also on conditions that favour or limit seedling recruitment across forest types

Geography and ecology shape the phylogenetic composition of Amazonian tree communities

Aim: Amazonia hosts more tree species from numerous evolutionary lineages, both young and ancient, than any other biogeographic region. Previous studies have shown that tree lineages colonized multiple edaphic environments and dispersed widely across Amazonia, leading to a hypothesis, which we test, that lineages should not be strongly associated with either geographic regions or edaphic forest types. Location: Amazonia. Taxon: Angiosperms (Magnoliids; Monocots; Eudicots). Methods: Data for the abundance of 5082 tree species in 1989 plots were combined with a mega-phylogeny. We applied evolutionary ordination to assess how phylogenetic composition varies across Amazonia. We used variation partitioning and Moran\u27s eigenvector maps (MEM) to test and quantify the separate and joint contributions of spatial and environmental variables to explain the phylogenetic composition of plots. We tested the indicator value of lineages for geographic regions and edaphic forest types and mapped associations onto the phylogeny. Results: In the terra firme and várzea forest types, the phylogenetic composition varies by geographic region, but the igapó and white-sand forest types retain a unique evolutionary signature regardless of region. Overall, we find that soil chemistry, climate and topography explain 24% of the variation in phylogenetic composition, with 79% of that variation being spatially structured (R$^{2}$ = 19% overall for combined spatial/environmental effects). The phylogenetic composition also shows substantial spatial patterns not related to the environmental variables we quantified (R$^{2}$ = 28%). A greater number of lineages were significant indicators of geographic regions than forest types. Main Conclusion: Numerous tree lineages, including some ancient ones (>66 Ma), show strong associations with geographic regions and edaphic forest types of Amazonia. This shows that specialization in specific edaphic environments has played a long-standing role in the evolutionary assembly of Amazonian forests. Furthermore, many lineages, even those that have dispersed across Amazonia, dominate within a specific region, likely because of phylogenetically conserved niches for environmental conditions that are prevalent within regions

Geography and ecology shape the phylogenetic composition of Amazonian tree communities

AimAmazonia hosts more tree species from numerous evolutionary lineages, both young and ancient, than any other biogeographic region. Previous studies have shown that tree lineages colonized multiple edaphic environments and dispersed widely across Amazonia, leading to a hypothesis, which we test, that lineages should not be strongly associated with either geographic regions or edaphic forest types.LocationAmazonia.TaxonAngiosperms (Magnoliids; Monocots; Eudicots).MethodsData for the abundance of 5082 tree species in 1989 plots were combined with a mega-phylogeny. We applied evolutionary ordination to assess how phylogenetic composition varies across Amazonia. We used variation partitioning and Moran's eigenvector maps (MEM) to test and quantify the separate and joint contributions of spatial and environmental variables to explain the phylogenetic composition of plots. We tested the indicator value of lineages for geographic regions and edaphic forest types and mapped associations onto the phylogeny.ResultsIn the terra firme and várzea forest types, the phylogenetic composition varies by geographic region, but the igapó and white-sand forest types retain a unique evolutionary signature regardless of region. Overall, we find that soil chemistry, climate and topography explain 24% of the variation in phylogenetic composition, with 79% of that variation being spatially structured (R2 = 19% overall for combined spatial/environmental effects). The phylogenetic composition also shows substantial spatial patterns not related to the environmental variables we quantified (R2 = 28%). A greater number of lineages were significant indicators of geographic regions than forest types.Main ConclusionNumerous tree lineages, including some ancient ones (>66 Ma), show strong associations with geographic regions and edaphic forest types of Amazonia. This shows that specialization in specific edaphic environments has played a long-standing role in the evolutionary assembly of Amazonian forests. Furthermore, many lineages, even those that have dispersed across Amazonia, dominate within a specific region, likely because of phylogenetically conserved niches for environmental conditions that are prevalent within regions