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Seeking to understand the origin of the forest

In a joint effort to explain the biological diversity of Amazonia and the Atlantic Forest, biologists and geologists have created the new field of geogenomics

Dried and pressed branches are stored as records of plant species, like this Pyrostegia venusta

Léo RamosDried and pressed branches are stored as records of plant species, like this Pyrostegia venustaLéo Ramos

For as much as biologists explore the ground, trees and bodies of water, they still appear to be far from gauging and explaining the biological diversity of the tropical forests. And by the same token, there is no explanation for how and when mountains, rivers and everything that lies beneath the forest emerged. Projects focused on Amazonia and the Atlantic Forest are now searching for answers: biologists and geologists are joining forces to find a way to decipher that history, in a field that geologist Paul Baker of Duke University labeled geogenomics in 2014. This new field of study has been given significant impetus by the collaboration between the Biota-FAPESP program and Dimensions of Biodiversity, a program of the National Science Foundation (NSF), the principal science funding agency in the United States. “Projects of this nature require a participatory approach from the time the questions are first being hammered out,” comments botanist Lúcia Lohmann of the Biosciences Institute at the University of São Paulo (IB-USP). Lohmann and American ornithologist Joel Cracraft of the American Museum of Natural History head the first project to cement such a partnership, focused on Amazonia.

In order to assemble the teams, they first needed to overcome basic barriers to communication. “A geologist would give a talk, and the biologists would be lost,” Lohmann says. And the opposite was also true. “At the first meeting, we spent two hours explaining a single slide to the geologists,” recalls biologist Cristina Miyaki, also from IB-USP, who heads a similar project that focuses on the Atlantic Forest. Once a common vocabulary was established, the exchanges began to take shape. “Now it’s clear that projects of this nature need to have researchers from both fields from the outset, but that wasn’t the perspective before we started,” Lohmann says.

Another nontrivial obstacle to consolidating knowledge is the scarcity of data. “We need to have all the phylogenies dated, with georeferenced databases, in order to produce distribution maps before we can cross-reference with the geological data,” Lohmann notes. She and her colleagues have planned a trip to the Amazon for 2016. “We’re going to collect data from different organisms to assess the extent to which the Negro and Branco rivers present barriers to dispersal.”

One can easily imagine that rivers carrying large volumes of water would limit the movement of organisms, but when biologists use DNA to retrieve information on the history of a species, that is not always what they see. “Rivers do not appear to be significant barriers to plants,” says Lohmann, who specializes in the family Bignoniaceae. But primate mobility may be limited in such cases, as shown by Brazilian primatologist Jean Philippe Boubli at the University of Salford, in England. He is also a researcher at the National Institute for Research on the Amazon (INPA), which allows him access to that institution’s large collection of primate samples. “We have nearly full coverage of samples of Amazonian primates, and with genomics we’ll be able to investigate the role of the major rivers in the origin primate diversity,” he says, looking ahead. With a new phylogeny for New World titi monkeys (Callicebus), published in March 2016 in the journal Frontiers in Zoology, Boubli, his doctoral student Hazel Byrne and colleagues cite deep divergences that justify the creation of two new genera: Cheracebus, for species from the Negro and Orinoco rivers, and Plecturocebus, in southern Amazonas State. Callicebus would be reserved for species from the Atlantic Forest. “They may be the key to everything,” Boubli says. It’s a very old, species-rich group, and therefore ideal for testing the role of factors such as rivers and climate change in species diversification. “The collaboration with geologists is opening our eyes to things we didn’t know about Amazonia,” he comments.

“What is becoming clear is that the theories advanced in recent decades are turning out to be overly simplistic for the complexity of the Amazon,” says biologist Camila Ribas of INPA, who is involved in both Lohmann’s and Baker’s projects. “The refuge theory holds that the present-day species originated during the glacial cycles, the last of which occurred about 18,000 years ago,” she notes. But the different regions of Amazonia appear to have gone through distinct processes, and species respond differently to local conditions. Birds, which are Ribas’ specialty, are a good example of organisms that are highly heterogeneous in coping with the environment: the ones that can fly long distances, for example, are less affected by barriers. At the opposite extreme, trumpeters (genus Psophia)—Amazonian birds that almost never fly—have become the prime example of how major rivers function as the principal barriers between species, according to a study published in 2012 in the Proceedings of the Royal Society B by Ribas and colleagues.

More recently, one of Ribas’ projects has researched the avifauna typical of the white sands areas of Amazonia, as described in a 2016 paper published in the journal Biotropica—the product of her student Maysa Matos’ master’s research. “These areas feature patches of white sand in the midst of a sea of forest, with open vegetation more akin to that of the Caatinga scrubland or the Cerrado savannah,” Ribas explains. What surprises is that the animals found in distant patches are more similar than you might imagine, even if they are unable to travel through the forest. The findings elicit a number of questions, such as how long that environment has existed and whether the forest was more permeable to those animals in the past.

During his master’s studies, another of Ribas’ students, Leandro Moraes, analyzed the role played by the Tapajós and Jamanxim rivers, in the state of Pará, in limiting the distribution of amphibians and reptiles. The findings, to be published soon in the Journal of Biogeography, show that the movement of one-third of amphibian species is limited by rivers; in the case of snakes and lizards, the percentage falls to just 8%. The paper focuses on assessing the importance of these rivers in the configuration of the landscape and the habitats suitable for these animals, and for this reason Ribas considers it to be an example of how the project is beginning to integrate areas of knowledge.

...and Cebus olivaceus ...

Anselmo d’AfonsecaLarge rivers limit the distribution of species such as Cebus olivaceusAnselmo d’Afonseca

Changing landscape
In recent years, the notion has begun to solidify that the Amazon Basin drainage network evolved predominantly in the last three million years (as opposed to 15 million, as earlier estimates claimed). That timescale appears to agree with indications from animal and plant data. The Isthmus of Panama—another structure of major importance to biogeography because it enabled migrations between South and Central America and the North—has also undergone an age change. A study led by geologist Camilo Montes of the University of the Andes, in Colombia, published in Science in April 2015, analyzed minerals of Panamanian origin found in South America and estimated the isthmus to be between 13 million and 15 million years old—10 million years older than was earlier thought. “The new dating results completely change how we see the past movement of flora and fauna in the region, and this is forcing us to reassess all of the literature,” says Lúcia Lohmann.

This reassessment has proven to be more productive because of the combined efforts of specialists. “Evolutionists and biogeographers need to know the geological history in order to understand why species live where they live, and even how species came to exist,” explains Paul Baker, who invented the term “geogenomics.” He has an ambitious plan to bore five drill holes near large Amazonian rivers at depths of up to two kilometers, to have continuous access to sediment samples of various ages, up to 65 million years old. At a 2015 meeting at INPA, he and colleagues from the Amazonia project reached an agreement on which types of data from this initiative might help reconstruct the geological, climatic and biotic history. The challenge now is to obtain funding. “Our budget for drilling alone is $7 million,” he says.

Baker’s project starts from a geological perspective, while in Lohmann’s project the questions spring chiefly from biology. Geogenomics, however, assumes a two-way street. “The idea is that geologists also use biological data to answer geological questions,” he says. The estimated dates for the emergence of the various trumpeter species studied by Ribas, for example, can help in estimating the age of major rivers such as the Amazon, the Xingu, the Tapajós and the Madeira, according to Baker.

“Biological data provide an order of magnitude that enables us to develop hypotheses we can test against the absolute ages derived from geochronological dating,” says sedimentologist Renato Almeida of the USP Geosciences Institute (IGc-USP). He and his colleague André Sawakuchi are investigating the formation of the sedimentary deposits that form the Amazon Basin. “It’s a continent-sized area on which data are absurdly scarce,” he says. The task of reducing this knowledge gap cannot be completed within the timeframe of the current project, and most of the data that the group is compiling has yet to be published. One of the team’s missions, in addition to painting a geographic picture of the past, is to help biologists distinguish which hypothesis offers the most firmly grounded explanation of the biogeographic patterns.

...but not of plants whose seeds are carried by the wind

Léo Ramos…but not of plants whose seeds are carried by the windLéo Ramos

The research efforts have been showing that the uplift of the Andes Mountains gradually pushed the water of an immense lake in that region towards the east, forming the large-scale drainages in the direction of the Atlantic Ocean. One technique for revealing the past of the rivers is optically stimulated luminescence, which relies on the collection of sediments from the steep banks that line the rivers, using aluminum tubes. “Back in the laboratory, we can determine the date when a grain of quartz was last exposed to sunlight,” explains geographer Fabiano Pupim, a postdoctoral researcher in Sawakuchi’s laboratory. The group is also discovering a wealth of information about the configuration of the sediments on the steep slopes adjacent to the rivers, which rise as high as 20 meters. Their internal structures allow scientists to infer the scale and direction of the river when the sediment was deposited, as well as other information.

Sonar images show that the bottoms of rivers like the Amazon—another unknown territory—have dunes as high as 12 meters. “We need to understand how a river of that size functions in order to infer what the great rivers of the past were like,” Almeida says. In collaboration with geologist Carlos Grohmann of the Institute of Energy and Environment at USP (IEE-USP), he is also looking into river dynamics using satellite image time series.

The rivers’ importance goes beyond their function as barriers. The streams and sediments that came from the Andes formed the environmental mosaic typical of Amazonia, which has some areas that are dry and others characterized by periodic flooding. Sawakuchi, Pupim and their team (in particular master’s students Dorília Cunha and Diego Souza) have investigated the formation of the Anavilhanas and Tabuleiro do Embaubal Archipelagos in the Amazon River over the last 10,000 years. The emergence of this type of environment and of the rivers themselves signifies distinct timescales, whose significance the geographer hopes to complement with the biological data.

In a laboratory illuminated only by red light, one can find out when sediment last received sunlight

Léo RamosIn a laboratory illuminated only by red light, one can find out when sediment last received sunlightLéo Ramos

Climate variation
But forests do not live from terrestrial water alone. Francisco William da Cruz Júnior of IGc-USP, a co-coordinator of the geology component of Brazilian geogenomics, uses speleothems—carbonate formations in caves—and stalagmites in particular, to infer past climate. The data obtained by his research group indicate that the Ice Age in South America was not arid, as scientists had thought. “Part of the continent was dry, but other areas were moist and may have even been conducive to expansion of the forests, such as in the Peruvian Amazon and the southern Atlantic Forest,” he notes.

Based on an analysis of oxygen isotopes contained in the calcium carbonate in cave material, he observes that different parts of Amazonia and adjacent regions went through very distinct processes. Evidence of these processes appears in a 2013 article in Nature Communications that he coauthored with biologists on the team, for which the lead author was his Chinese colleague Hai Cheng. The dating results indicate that in the last 250,000 years, the climate in western Amazonia was more stable than that of the area to the east, in the state of Pará, which received intensified rainfall during the glacial periods—between 100,000 and 20,000 years ago. The group interprets this relative stability as being responsible for the high biodiversity found in the region today, while the less species-rich eastern Amazonia experienced drastic climate variation that may have led to extinctions. “We are challenging a paradigm,” says Cruz. “Climate stability may have been more important than refugia in creating the pattern of high diversity found today in the Amazon forest, particularly near the Andes.”

During the glacial period, western Amazonia appears to have been quite moist, like the Atlantic Forest region in southern and southeastern Brazil. Cruz has found evidence of a climate belt that connects these two regions and has features contrasting with those found in the area that includes Pará, in eastern Amazonia, and the Northeast, where the climate varies in cycles of about 23,000 years. “That pattern is being tested in both the Amazonia project and the Atlantic Forest project.” He maintains that these correspondences enabled the formation of corridors between the two biomes, which explain cases of closer kinship between species of Amazonia and the Atlantic Forest, as compared to species within the same biome. Cruz postulates that in a period in which high moisture is hypothesized in eastern Amazonia and Northeastern Brazil, the tropical forests are likely to have expanded, forming a forest bridge between the two biomes. Later on, there are signs of more abundant rainfall in the region closer to the foot of the Andes and in the Brazilian South and Southeast, where the forests also may have expanded until Amazonia and the Atlantic Forest came together. “We are currently testing what these phases might have been.”

Layers of a stalagmite ...

Léo RamosLayers of a stalagmite …Léo Ramos

Evidence of this dynamic comes in the form of the fossilized leaves collected by Cruz in the valley of the São Francisco River, a region now covered by Caatinga vegetation. “They indicate that the region was quickly covered by moist vegetation between 18,000 and 15,000 years ago,” he says. Even now, there is a direct climate connection between the two biomes: in summer, the moisture that travels from Amazonia determines what happens in the Atlantic Forest, for example. “You can’t restrict the study to a local scenario; it’s not interesting,” Cruz says.

The Atlantic Forest project, begun a year after the Amazonia project and led by biologists Cristina Miyaki of USP and Ana Carolina Carnaval of the City University of New York, is at an earlier stage of specialty integration. “Several papers we are working on in this third year include the angle or hypothesis that the team of paleoclimatologists (or the remote sensing team) found for our team,” Carnaval says. A paper with genomic data which test theories formulated by Cruz and other members of the geology team—such as palynologist Marie-Pierre Ledru of the Institute of Evolutionary Sciences of Montpellier, France—is being finalized for publication. “It’s really cool because paleoclimatology points to a path, and genomics then tests it and sees what agrees, and what doesn’t agree,” she says. “Then we bring the discussion back to the paleoclimatologists to refine the ideas.”

...and fossilized leaves are indicators of past climate

Léo Ramos…and fossilized leaves are indicators of past climateLéo Ramos

The findings are now coming to light, and they promise to be very fruitful in the next few years, when the current funding has been replaced by other projects. Firming up the partnership is, it seems, the biggest victory. “We’re beginning to delineate what is not yet understood,” says Miyaki. Her work has always involved assumptions from the field of geology to understand the diversification of birds in the Atlantic Forest. But now, with the new lessons learned, comes the feeling that the analyses were very superficial and that the interpretations, though they were the best ones possible at the time, were naive.

Geogenomics is an example of the best of modern science. “In a certain way, we’re going back to the natural history of old, when researchers had an understanding of biology and geology,” Miyaki jokes. But, with ever more specialized techniques, increasingly massive databases and a growing level of detail, the only way to bring this knowledge together is to assemble large groups. Now that the researchers have moved past the initial years when each specialty continued to produce papers similar to their earlier ones, the truly integrated findings should really begin to appear.

Projects
1. Structure and evolution of the Amazonian biota and its environment: an integrative approach (nº 2012/50260-6); Grant Mechanism Biota Program/Dimensions-NSF; Principal Investigators Lúcia Lohmann (IB-USP) and Joel Cracraft (AMNH); Investment R$3,752,671.77.
2. Dimensions US-Biota São Paulo: a multidisciplinary framework for biodiversity prediction in the Brazilian Atlantic Forest hotspot (nº 2013/50297-0); Grant Mechanism Biota Program/Dimensions-NSF; Principal Investigators Cristina Miyaki (IB-USP) and Ana Carolina Carnaval (CUNY); Investment R$3,781,927.16.

Scientific articles
BAKER, P. A. et al. The emerging field of Geogenomics: Constraining geological problems with genetic data. Earth-Science Reviews. V. 135, p. 38-47. August 2014.
BYRNE, H. et al. Phylogenetic relationships of the New World titi monkeys (Callicebus): First appraisal of taxonomy based on molecular evidence. Frontiers in Zoology. V. 13, No. 10. March 1, 2016.
CHENG, H. et al. Climate change patterns in Amazonia and biodiversity. Nature Communications. V. 4, No. 1,411. January 29, 2013.
MATOS, M. V. et al. Comparative phylogeography of two bird species, Tachyphonus phoenicius (Thraupidae) and Polytmus theresiae (Trochilidae), specialized in Amazonian White Sand Vegetation. Biotropica. V. 48, No. 1, p. 110-20. January 2016.
MORAES, L. J. C. L. et al. The combined influence of riverine barriers and flooding gradients on biogeographical patterns for amphibians and squamates in south-eastern Amazonia. Journal of Biogeography. In production.
RIBAS, C. C. et al. A palaeobiogeographical model for biotic diversification within Amazonia over the past three million years. Proceedings of the Royal Society B. V. 279, No. 1,729, p. 681-9. January 11, 2012.