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Zoology

Direct flight

Kinship between birds reveals a connection between the Amazon and Atlantic forests at two moments in the past

In both biomes: male Red-headed Manakins attract females with coordinated dances

TOMAZ MELO/FEDERAL UNIVERSITY OF ACREIn both biomes: male Red-headed Manakins attract females with coordinated dancesTOMAZ MELO/FEDERAL UNIVERSITY OF ACRE

An analysis of the kinship between dozens of bird species of the Atlantic and Amazon forests has led biologist Henrique Batalha-Filho to identify two periods in the distant past in which these two ecosystems, now separated by distances of up to 1,500 kilometers, were connected. The two Brazilian forests are home to small birds—black with a scarlet head, nut-brown with white and gray spots, among other descriptions—that have various degrees of kinship, indicating some type of physical connection between the two environments at different times. The long-ago connection had already been revealed in prior studies of plants and mammals, but until now, no one knew when, or which tracts of the forests had been in contact.

This information has begun to crystallize on the basis of research that Batalha conducted on passerine birds of the New World suboscine group. The most well-known representatives of this group in Brazilian cities are birds of the tyrant flycatcher family and the Ovenbird. Batalha did not work with these two species, but rather with birds of the same forest-specialized group, such as the Spotted Bamboowren (Psilorhamphus guttatus), which lives in the Amazon Forest, the Rusty-belted Tapaculo (Liosceles thoracicus) of the Atlantic Forest, and the Screaming Piha (Lipaugus vociferans), found in both forests. According to Batalha’s findings, published in January 2013 in the print edition of the Journal of Ornithology, the great-great-great grandmothers of the great-great-great grandmothers of the passerines whose calls are heard today in both areas came into contact and left descendants as a result of geological and ecological events at two very distinct moments.

Southern route
Batalha estimates that the older of those two moments occurred during the Miocene Epoch, between 23 million and 5 million years ago, when the Pacific Tectonic Plate collided with the South American Plate, lifting the Andes into a mountain range more than 7,000 kilometers long with an average altitude of 3,500 meters that cuts through seven countries—Chile, Bolivia, Peru, Ecuador, Colombia, Argentina and Venezuela. The mountains that rose up and formed a high wall isolating Amazonia from the Pacific Ocean also created elevated channels where flooded savannahs formed, and these could have acted as bridges between the southwestern part of Amazonia, which is now the state of Rondônia, and the Atlantic Forest in what is now southern and southeastern Brazil. That temporary bridge, which must have been similar to the Chaco region distinctive of Paraguay and Bolivia, enabled birds to move around despite the more arid environment that now isolates the two forests.

The witnesses to this ancient connection are the Spotted Bamboowren commonly found in the bamboo thickets of the Atlantic Forest, which is 13 centimeters long with scattered spots, and the Rusty-belted Tapaculo, known for its strident call and found in the Amazonian floodplains. Batalha explains that the existence of very similar species—sister species, in biologists’ jargon—each exclusive to one of the two biomes is evidence of an older connection, after which there was sufficient time for the birds to differentiate. Even more eloquent examples of this divergence, the researcher notes, are found in the sister genera Mackenziaena and Frederickena. The genus Mackenziaena is represented by Antshrikes and Large-tailed Antshrikes, 22-centimeter-long passerines with red irises. The Black-throated Antshrike and the Undulated Antshrike, both of the genus Frederickena, in turn, are typical of Amazonia. The existence of genera exclusive to each of the two forests purportedly indicates that, when the southern route disappeared, birds with a common ancestor remained isolated to the east and to the west, and over time their descendents accumulated enough differences to merit that taxonomic distinction.

Northern route
The second linkage occurred more recently, during the Pliocene and Pleistocene, between 5.5 million and 11,500 years ago, when the Atlantic Forest along the northeastern coast was joined with the Amazonian vegetation of the Guianas and the Brazilian state of Pará near Marajó Island, as well as the areas around the Xingu and Tocantins-Araguaia rivers. According to Batalha, the principal factor in this region that influenced species differentiation were glaciations. To justify this analysis, he turns to the Refuge Theory developed in the 1960s by German biogeographer Jurgen Haffer and applied to Amazonian evolution by Brazilian zoologist Paulo Vanzolini in the early 1970s (see Pesquisa FAPESP No. 208).

 Antshrike: male photographed in Piraju, in inland São Paulo State

DARIO SANCHESAntshrike: male photographed in Piraju, in inland São Paulo StateDARIO SANCHES

According to this model, during periods with a colder, dryer climate on much of the American continent, there were surviving forest fragments where birds sought shelter and came into contact. “In glaciations, dry regions tend to expand and forests shrink,” Batalha explains. “But precipitation increased during the Pleistocene in some sections of the Caatinga, as indicated by larger calcium deposits in cave stalactites and stalagmites.” This increased rainfall resulted in the emergence of an area where birds were able to survive—an intermediate forest between the moist forests and the Caatinga that today occupies the northeastern sertão.

One strong indication of this more recent linkage is the existence of species that live in both the Amazon and the Atlantic Forest, but not in the arid band that separates the two. Examples include the gray-brown Screaming Piha, which is 25 centimeters in length and acts as a forest sentinel, and the Red-headed Manakin (Pipra rubrocapilla), the males of which show off in coordinated dances to attract the females during the mating season.

“We know that in both the Miocene and the Pleistocene these contacts occurred more than once, although it’s impossible to estimate how long the birds were in proximity,” Batalha acknowledges. He now dedicates his time to understanding the direction in which these migrations took place. The data, which are still preliminary, indicate that along the southern route, the movement appears to have been bidirectional, because older species are found in both the Amazon and the Atlantic Forest. Along the northern pathway, the birds probably flew more actively from west to east, because the older populations are primarily in Amazonia. “The important thing is that we were able to develop the first model that takes into account time and space to show, on the basis of the species evaluated, that the two biomes had been connected in the past, and also suggests the forces that caused them to separate.”

Batalha explains that New World suboscines are excellent for this type of study because they have been present throughout the entire geological history of South America. Ancestors of this group already existed when the continent separated from Africa about 100 million years ago, and here they diversified and differentiated from their Old World relatives. “In addition to being representative of the two biomes, this group of birds has also been widely studied, which has enabled us to do more extensive analyses,” he concludes. For his research, Batalha used genetic data stored in GenBank, a public database.

To do the research for the Journal of Ornithology article, a component of his doctoral studies, he spent three months at the Natural History Museum of Denmark in Copenhagen. There he worked with Jon Fjeldså, curator of the bird collection and a specialist in species of the Andes. “He was the one who came up with the idea of comparing phylogenetic and geographic data, and this was a decisive factor in our ability to observe the connecting routes between the Atlantic and Amazon forests,” Batalha observes.

In comparing certain sections of DNA of the species under study, he analyzed the genetic similarity between them, as well as their hierarchical relationships (which ones were older and which were more recent). “Starting from the present-day similarities and finding out the percentage of mutations that occurred during each specific period of time for each family, we were able to retrospectively arrive at the common ancestor,” he explains. “That’s how we confirmed that these birds were together in the past.”

Ana Paula CamposOnce the connections were proven, they further needed to understand when the birds came into contact—and why they ultimately separated. The answers came from the available literature on other transformations of the continent. “There are well-known articles, for example, that uncover the geological relationships between the Atlantic Forest and the Amazon based on analysis of ancient pollen and cave stalactites,” says Cristina Miyaki, his research advisor. “The principal breakthrough offered by the study was the development of a large-scale meta-analysis in which we looked at several factors. We were able to connect phylogenetic, geological, climatic and geographic distribution data, which enabled us to give a more detailed description of what happened over time,” Miyaki comments.

These contributions augment the scenario outlined by previous studies. Batalha took inspiration in part from the work of biologist Leonora Costa of the Federal University of Espírito Santo, published in 2003 in the Journal of Biogeography. During her doctoral studies at the University of California at Berkeley, Costa charted ambitious transects through Brazil from the Atlantic Forest to Amazonia. Along a stretch hundreds of kilometers long she captured small mammals, mainly rodents and marsupials, and analyzed their DNA to investigate the evolutionary relationships between the species. Surprised to find many cases in which species of the Atlantic Forest had relatives in the Amazon that were more closely related than those within the Atlantic Forest, she conceived links between the two forests, represented today by gallery forests along the rivers of the Cerrado, and moist enclaves known as brejos, in the Caatinga. “I interpreted the animals that ‘were left’ in these locales as clues to past links that no longer exist today,” Costa explains.
The more elaborate scenario outlined by Batalha could help inspire new studies that will further reveal the dynamics of flora and fauna formation in the Brazilian forests through the ages.

Project
Reconstruction of the evolutionary history and phylogeographic studies of neotropical birds based on molecular markers II (nº 2009/12989-1); Grant mechanism Regular Line of Research Project Award; Coord. Cristina Yumi Miyaki/IB-USP; Investment R$230,021.25 (FAPESP).

Scientific article
BATALHA-FILHO, H. et al. Connections between the Atlantic and the Amazonian forest avifaunas represent distinct historical events. Journal of Ornithology. v. 154, n. 1, p. 41-50. Jan. 2013.

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