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Cycle 5 (2015 Deadline)

History and diversification of floodplain forest bird communities in Amazonia: towards an integrated conservation plan

PI: Camila Ribas (, Instituto Nacional de Pesquisas da Amazonia (INPA), Ministry of Science, Technology, and Innovation, and co-PI Alexandre Aleixo, Museu Paraense Emílio Goeldi (MPEG)
U.S. Partner: Joel Cracraft, American Museum of Natural History
Project Dates: December 2016 - November 2019

Project policy brief on Amazon dams, October 2020 (English)          Dossie politico sobre barragens amazônicas, Outubro de 2020 (Portuguese)

Project Overview:

This research project is crucial, given that Amazonian countries are focusing on building hydroelectric dams, which will impose a significant impact to the biota specialized in flooded habitats through habitat loss, fragmentation, and changes in sediment dynamics. This biota has a unique, complex, and still poorly known history, as wetlands probably dominated western Amazonia for a large portion of the Neogene, and significant changes on the drainage pattern have occurred since then. Although birds are one of the best-known groups of vertebrates, flooded habitat bird assemblages are still poorly known and have been very little explored using molecular techniques. Based on the dynamic history of flooded habitats (with their frequent cycles of building and erosion due to sedimentary processes), bird species from these habitats were assumed to have high dispersal ability and consequently to lack genetic structure. However, recent studies of phenotypic and genomic variation have shown that this is not the case. Substantial cryptic diversity and endemism have been found within some of these taxa, which indicates that patterns and processes underlying these patterns are not well understood. Within the context of the developmental plans for energy generation, this constitutes a major threat to a significant portion of Amazonian biodiversity that is little known. Dr. Ribas and her colleagues will generate a multidisciplinary dataset, including genomic, ecologic, and spatial biotic and abiotic data that will be integrated to (1) advance our knowledge on the evolution of Amazonian flooded habitats and their biota and (2) provide information that can be used for assessing the impact of proposed hydroelectric dams and for identifying areas of conservation priority. This will be accomplished in collaboration with the NSF-funded project led by Dr. Cracraft, which aims to reconstruct the history and evolution of the Amazonian biota and its environment, focusing mainly on the upland forest biota, and will provide background information on methods and analysis, as well as complementary data.

Hydroelectric energy generation is considered a source of clean and renewable energy, but current environmental impact assessments ignore the long-term irreversible impacts that dams have on Amazonian flooded habitats. There are 121 established, and 303 planned, dams for the Amazon region, most of them in Brazil. In the Amazonian lowlands, 51 dams already exist and 130 more are planned. Among the ten largest planned dams, three are built or nearing completion: Santo Antônio and Jirau (Madeira River) and Belo Monte (Xingu River). The remaining seven are still in planning stages, reinforcing the need for immediate attention to the impacts of these projects. Most planned dams in the Amazonian lowlands will adopt the “run of the river” system, in which large extensions of flooded habitat are kept permanently flooded, submerging river islands and disrupting the hydrologic cycle. The resulting loss of species in flooded habitats may impact the upland biota as well, as taxa from both habitats are interconnected by ecological processes, and thus have important consequences for large portions of Amazonian protected areas and indigenous lands, affecting availability of resources for both the ecosystem and traditional and indigenous communities. To assess the impact of planned dams on the Amazonian biota it is essential to understand the history and distribution of flooded habitats’ biological diversity, as well as the importance of the hydrological cycle in developing and maintaining this diversity. For this, an interdisciplinary framework is necessary that considers the evolution of the current landscape and its possible responses to the dams. Dr. Ribas has assembled a multidisciplinary team that will study population genomics, ecological affinities, biological diversification, and species distribution patterns for flooded habitat birds and relate these patterns to spatial distribution and chronology of flooded habitats, sediment dynamics responsible for building or erosion of flooded substrates, and hydrology of the most threatened Amazonian basins. As a result, they expect to produce and disseminate data and integrative analytical methods that will inform environmental impact assessments related to planning and execution of developmental projects taking place in the future and especially over the coming decade in Brazil.

5-009 Toucan5-009 Sample Analysis
The team conducted field expeditions to gather samples from a number of species.Following data collection, the team organized and collated collected samples (photo courtesy of Dr. Ribas).

Final Summary of Project Activities 

This project relied on a combination of basic data collection and analyses from different disciplines, with the aim of combining basic results to achieve integrative results and provide two main outcomes, with impacts on policy and planning. Below are sections summarizing progress made on the various key aspects of the project. An important result that permeates the entire project is the support provided for student projects and thus for the development of new researchers in Amazonia. The project has supported data collection for 14 graduate students, 10 of them enrolled in graduate programs from Amazonian research institutions. This impact of the project is quite timely and relevant, as the PI and her colleagues have helped to build the skills and capacity of new researchers in a region that is poorly known, greatly threatened, and urgently in need of more locally based scientists.

Basic Analysis:

1- Mapping flooded habitats
Mapping the different Amazonian habitats is challenging, due to the homogeneous relief, heterogeneity and seasonality of habitats, lack of field data to confirm habitat classifications, and intense cloud cover. Dr. Ribas and her colleagues worked to update the best previous map of Amazonian wetlands, which was published by Hess et al. in 2015, based on images acquired in 1995-1996. Due to its low resolution and to the fact that it applies the same high and low water season for the whole Amazon basin, one of their objectives was to update this map so that they could infer available habitat for bird species associated to different kinds of flooded habitats. Dr. Thiago Silva led this effort, which proved to be quite challenging. Dr. Silva and his team started from the Hess et al. (2015) map and refined it using ALOS/PALSAR images (resolution of 12.5 meters). Then they developed a habitat classification scheme in four vegetation classes (herbs, shrubs, open formation, flooded forest) and incorporated information on water color (white water, clear water, black water) compiled from Pekel et al. (2016). They collected ground data in joint field expeditions to extract training samples of the major habitat classes. They also developed a platform for gathering ground truth information for different regions visited by other team members. Classification was finalized in a region spanning central Amazonia, from Manaus to Tefé, and they are now working on expanding the classification to the rest of Amazonia. This effort took longer than expected due to several difficulties in hiring technicians for remote sensing analyses and to the fact that Dr. Silva changed institutions in the beginning of 2019, moving to another country (UK). Alternatives were sought by establishing a partnership with Dr. Hanna Tuomisto (University of Turku, Finland) and her group, who developed a Landsat mosaic for Amazonia. One of the PhD students on the project spent six months in her lab and is using the Landsat mosaic for analyzing genomic population data.

2- Mapping Species Distributions
The PI and her team had two graduate students (Dr. Thiago Laranjeiras and MSc. Jadson Viana) working on compiling occurrence data for bird species associated to seasonally flooded habitats and analyzing the patterns of distribution, diversity, and endemism. Both defended their thesis/dissertation and are preparing the manuscripts for submission. The results obtained were already used to inform Ibama (the Brazilian Institute of Environment and Renewable Natural Resources) in its technical report about the impacts of Belo Monte dam in the Xingu River, and to provide information to ICMBio (the Chico Mendes Institute for Biodiversity Conservation) in the analysis of the impact assessment studies for the Bem Querer dam in the Branco River. Dr. Laranjeiras works at ICMBio and thus continues direct involvement in planning for hydropower production in Amazonia. The main basic result of this step was successfully obtained and is being used to inform the remaining analyses.

3- Genomic Analysis
The PEER team originally selected 32 species associated with the different seasonally flooded habitats for which they had reasonable sampling already deposited in tissue collections in Brazil (INPA and MPEG) and abroad (LSUMNS, AMNH, FMNH, NMNH, ANSP). Additional samples were collected during the project. They obtained genomic data using UCE probes for all these taxa, plus eight additional species (total of 40 species, 786 samples sequenced so far). Two graduate students (Dr. Gregory Thom and MSc. Matheus Carvalho) finished their thesis/dissertation working with this genomic dataset, and Dr. Thom has published two papers from his PhD work. The team has results concerning intraspecific structure and genomic diversity for 35 species so far, which are under study by four ongoing graduate students and four postdocs or associate researchers. Intraspecific structure analysis has already revealed threatened taxa in the Branco, Xingu, and Madeira river basins. Genomic diversity and population history analyses are showing that Eastern Amazonian populations are often smaller and less diverse than Western populations, indicating a greater extinction risk when seasonally flooded habitats are suppressed in Eastern sub-basins.

4- Mapping permanent flooded areas by dams
This basic analysis was not yet complete as of the time the PEER project ended in November 2019, due mainly to difficulties in obtaining precise information about dam location and height from the assessments of hydropower potential made by the government. This will be needed in the final planning stage that Dr. Ribas and her group still plan to implement in partnership with governmental agencies.

5- Ecological analysis
To connect information on habitat distribution and bird population dynamics, we need to understand the habitat affinities of each species. Field data is crucial for that, but standardized ways of obtaining this data have long been debated. The PEER team decided to employ Passive Acoustic Monitoring (PAM), a relatively new approach, to generate data on habitat use for some of the species studied in the project. One of the PhD students, MSc Tomaz Melo, acquired PAM data in the four seasons of the hydrologic cycle in two sites along the Madeira River, one that was affected by the flooding caused by the Santo Antônio dam (completed in 2011) and another that lies downstream of the dam and has suffered little or no impact on vegetation structure and flooding cycle. Several different kinds of flooded habitat were targeted at each site. This study design was elaborated to understand both habitat affinities and bird usage of the habitats that result from the flooding caused by the dam. This will allows development a measure of sensitivity of each species, besides understanding their habitat use. Field work at the Madeira basin spanned 101 days, with a total of 182,994 recordings obtained. Species lists were built for each locality based on 3,200 randomly selected recordings. Vegetation data before and after the dam for each locality was obtained through Landsat images and plots at the field sites. The first manuscript is in preparation and should be submitted in January 2020. PAM data was also obtained along the mid-Xingu River, in the region affected by the Belo Monte dam. A total of 26,447 recordings were obtained and were used to inform the evaluation of the monitoring plan that is being executed by the consortium that manages the Belo Monte power plant.

Integrative Results:

6- Patterns of species distribution + areas of endemism
Based on the work of Dr. Thiago Laranjeiras and MSc Jadson Viana, the PEER team was were able, for the first time, to propose areas of endemism (AoE) for flooded forest Amazonian birds. These AoE differ significantly from the AoEs that have been described for upland forest birds and that usually guide conservation efforts. For the flooded habitats, the distinctive characteristic of the upper Madeira, upper Solimões, and Tocantins avifaunas indicate historical isolation of these areas and thus special attention to their conservation. The avifauna of the Branco River also stands out as unique, probably due to its historical relationship with the Orinoco basin, an important result considering that the impact assessment studies for the Bem Querer dam, at the Branco River, are ongoing. The results also show that the lower Xingu flooded habitats harbor an avifauna similar to the lower Amazon, while the medium and upper Xingu habitats harbor an avifauna similar to the Tocantins avifauna, which is also highly threatened by hydropower projects. Thus, this regionalization is a big advance in planning and understanding the impacts of damming Amazonian rivers, and has so far contributed to highlight areas of conservation priority, as proposed in the original project. It is important to note that the regionalization proposed takes into account the revised taxonomy obtained through the genomic analyses of the 35 taxa for which the team has already generated genomic data.

7- Habitat loss + fragmentation
Dr. Ribas and her group assessed the relationship between the temporal dynamics of flooded habitats and its relationship with the evolution of bird populations by conducting integrative studies using genomic data and sedimentary chronology of the flooded habitats. Luminescence dating of sediments is being used to constrain the evolution of flooded habitats along the Solimões (Pupim et al. 2019), Madeira, Xingu, and Amazonas rivers, and this information is being combined with population history obtained from genomic data and habitat affinities of taxa obtained through PAM. This facilitates a consideration of how past and future fragmentation of each kind of flooded habitat can potentially affect (or has potentially affected) the connectivity among bird populations. This discussion appears in one published (Choueri et al 2017) and one recently accepted study (Thom et al. in press, Science Advances). Another outcome of these studies is a general model of evolution for Amazonian habitats (Bicudo et al. 2019, Scientific Reports), and the general effects of dams on sedimentary dynamics in an integrated Amazonian scale (Latrubesse et al. 2017, Nature). Despite these results obtained so far, the team still aims to produce a prioritization analysis, integrating available data.

Although the PEER project has ended, Dr. Ribas and her colleagues will continue their collaboration with their USG-supported partners and other researchers to analyze and publish their data. In addition, the PI notes that a very interesting experience in this project was the interaction with indigenous and river dweller communities from the Xingu River basin, working with local researchers on collecting and analyzing scientific data and then using these results to sustain their arguments for better planning and management of the impacts to their territories. The PI wants to continue exploring the intersections between academic research on biodiversity and application of these results for protecting the environment in parallel to development projects. Partnership with local communities, especially indigenous communities, seems to be the strongest way of doing that. The effects of large infrastructure projects in Amazonia are soon to be combined with effects of climate change and land governance, as the Amazonian fires have shown in 2019. She emphasizes that we need to understand how natural populations react to changing environments in order to plan for these combined effects in the near future. Therefore, her plans for future research include using the datasets she and her team have built and combining them with more refined information on past, present, and future climate, as well as with information from the local communities about how these changes affect the different species in the distinct Amazonian habitats. As local researchers gather data and perform analyses, they will have the experience to discuss the impacts instead of being repeatedly just the objects of research.

Recent Papers Published:

Silva, S.M.; Peterson, A.T.; Carneiro, L.; Burlamaqui, T.C.T.; Ribas, Camila C.; Sousa-Neves, T.; Miranda, L.;  Fernandex, Alexandre M.; D'Horta, Fernando M.; Araujo-Silva, Lucas E.; Batista, R.; Bandeira, C.H.M.M.; Dantas, Sidnei; Ferreira, Mateus; Martins, D.M.; Oliveira, J.; Rocha, T.C.; Sardelli, C.H. Thom, Gregory; Rego, P.S.; Santos, Marcos Persio Dantas; Sequeira, F.; Vallinoto, M.N.; Aleixo, A.L.P. 2019. A dynamic continental moisture gradient drove Amazonian bird diversification. Science Advances vol. 5, p. eaat5752-10. DOI: 10.1126/sciadv.aat5752

Pupim, F.N.; Sawakuchi, Andre O.; Almeida, R.P. Ribas, Camila C.; Kern, A.K.; Hartmann, G.A.; Chiessi, C.M.; Tamura, L.N.; Mineli, T.D.; Savian, J.F.; Grohmann, C.H.; Bertassoli Jr., D.J.; Stern, A.G.; Cruz. F.W. Cracraft, Joel. 2019. Chronology of Terra Firme formation in Amazonian lowlands reveals a dynamic Quaternary landscape. Quaternary Science Reviews, vol. 210, p. 154-163, 2019.

Schultz, E.D.; Perez-Eman, J.L.; Aleixo, A.P.; Miyaki, C.Y.; Brumfield, R.T.; Cracraft, J.; Ribas, C.C. 2019. Diversification history in the Dendrocincla fuliginosa complex (Aves: Dendrocolaptidae): Insights from broad geographic sampling. Molecular Phyogenetics and Evolution, vol. 140, p. 106581, 2019.

Ribas, C.C., and Aleixo, A.P. 2019. Diversity and evolution of Amazonian birds: implications for conservation and biogeography. Anais da Academia Brasilieira de Ciencias ONLINE), v. 91, p. e20190218.

Bicudo, T.C.; Sacek, V.; Almeida, R.P.; Bates, John M.; Ribas, C.C. 2019. Andean Tectonics and Mantle Dynamics as a Pervasive Influence on Amazonian Ecosystem. Scientific Reports, vol. 9, p. 16879.

Zuanon, Jansen; Sawakuchi, Andre O.; Camargo, M. Wahnfried, I.; Sousa, L.; Akama, A.; Muriel-Cunha, J.; Ribase, Camila C.; D'Horta, Fernando M., Pereira, T.; Lopes, P.; Mantovanelli, T.; Lima, T.S.; Garzon, B.R.; Carneiro C.; Reis, C.P.; Rocha, G.; Santos, A.L.P.; Mileno, E.; Pennino, M.G.; Pezzuti, J. 2019. Conditions for the maintenance of seasonal flood dynamics, conservation of the aquatic ecosystem, and maintenance of the modes of life of the people of the Volta Grande do Xingu. Papers do NAEA (UFPA), vol. 28, p. 10, 2019.

Thom, Gregory; Xue, A.T.; Sawakuchi, Andre O.; Ribas, C.C.; Hickerson, Michael J.; Aleixo, A.P.; Miyaki, C.Y. Quaternary climate changes as speciation drivers in the Amazon Floodplains. Science Advances, in press (2019)..

Batista, R.; Olsson, Urban; Andermann, T.; Aleixo, A.P.; Ribas, Camila; Antonelli, Alexandre. Phylogenomics, biogeography and diversification of the world’s thrushes (Aves, Turdus): New evidence for a more parsimonious evolutionary history. Proceedings of the Royal Society B-Biological Sciences, in press (2019).

Cracraft, J.; Ribas, C.C.; d'Horta, F.M.; Bates, J.; Almeida, R.P.; Aleixo, A., Boubli, J.P.; Campbell, K.E.; Cruz, F.W.; Ferreira, M; Fritz, S.C.; Grohmann, C.H.; Latrubesse, E.M.; Lohmann, L.G.; Musher, L. J.; Nogueira, A.; Sawakuchi, A.O., Baker, P. The origin and evolution of Amazonian species diversity. In: Neotropical Diversification: Patterns and Processes, edited by Valentí Rull and Ana Carolina Carnaval, Springer, in press (2019).

Capurucho, J.M.G; Borges, S.H.; Cornelius, C.; Vicentini, A.; Prata, E.M.B.; Costa, F.M.; Campos, P.; Sawakuchi, A.O.; Rodrigues, F. ; Zular, A.; Aleixo, A.; Bates, J.M.; Ribas, C.C. Patterns and processes of diversification in Amazonian white sand ecosystems: insights from birds and plants. In: Neotropical Diversification: Patterns and Processes, edited by Valentí Rull and Ana Carolina Carnaval, Springer, in press (2019).

Moraes, L.J.C.L., Ribas, C.C., Pavan, D., Werneck, F. Biotic and landscape evolution in an Amazonian contact zone: insights from the herpetofauna of the Tapajós River basin. In: Neotropical Diversification: Patterns and Processes, edited by Valentí Rull and Ana Carolina Carnaval, Springer, in press (2019).

Silva, S. M., A.T. Peterson, L. Carneiro, T.C.T. Burlamaqui, C.C. Ribas, T. Sousa-Neves, … A. Aleixo. (2019). A dynamic continental moisture gradient drove Amazonian bird diversification. Science Advances, 5(7).  

Recent Press Releases (in Portuguese):  

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