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Snakes in a bind

A national mapping project indicates that, in just a few decades, some species have lost 80% of their territory

The golden lancehead viper, from Queimada Grande Island

Eduardo CesarThe golden lancehead viper, from Queimada Grande IslandEduardo Cesar

After four years organizing a rare synthesis of information produced during many decades of fieldwork, biologist Cristiano Nogueira can finally say: “Now we can see clearly that the main threat to Brazilian snakes is a dramatic loss of native vegetation, which is also the cause of other problems such as the drought in Sao Paulo.” As a researcher at the Zoology Museum of the University of São Paulo (MZ-USP), he coordinates an extensive mapping project, comparing the current and past geographical distributions of Brazilian snakes. Preliminary results indicate that some species have lost up to 80% of the forest area or fields that they occupied three decades ago. This loss of territory—associated with the expansion of cities, agriculture and livestock raising, and which also affects other species—has led to the disappearance of the evidence of the evolutionary history not only of snakes, but also of other animal groups that evolved and occupied their territories over millions of years.

In 2016 Nogueira expects to complete more than 1,000 maps precisely demarcating this problem by comparing the areas occupied today and in the past by the 380 species found in Brazil. This represents the greatest diversity of snakes in the world, including the tiny, inoffensive blind snakes, the jararacas or lanceheads, rattlesnakes, coral and false coral snakes, and the larger snakes, such as the boa and anaconda, reaching lengths of up to 10 meters. According to the maps already complete, 22 species are unique—or endemic—to the Caatinga scrubland and another 80 are unique or endemic to the Atlantic Forest. “We are discovering in which areas they are endemic and, at the same time, seeing that we are losing them,” observes Nogueira, who leads a team of 25 specialists from Brazil and two from Argentina.

Bothrops itapetiningae, the smallest of the jararacas, measuring 40 to 60 centimeters—the males have a longer tail, while females have a larger head—today occupies only about 20% of the territory it occupied 30 years ago, which extended throughout the fields and Cerrado savannahs from São Paulo to the center of the state of Goiás. This region has been heavily occupied by plantations or cities. “Deforestation has reached the edges of the Xingu Indigenous Reserve, in the states of Mato Grosso and Pará, and Emas National Park in Goiás,” says Nogueira. “The losses have increased a lot since I began this survey in 2010 and are now advancing towards the Amazon forest.”

The first records of Brazilian snakes: above, a chicken snake in a book published in Germany in 1734;

Thesauri / Albertus Seba The first records of Brazilian snakes: a chicken snake in a book published in Germany in 1734…Thesauri / Albertus Seba

Another species threatened is the Murici lancehead (Bothrops muriciensis), found only in forests at altitudes greater than 400 meters in an ecological park in the municipality of Murici, in Alagoas State. Marco Antonio de Freitas, a researcher at the Chico Mendes Institute for Biodiversity Conservation (ICMBio) who coordinated the fieldwork for this species, saw that deforestation is intense there, even in areas protected by law. That is not the only problem. “In the North and Northeast, educational efforts to prevent the killing of venomous snakes are not effective. The best we can do is convince residents to not kill those that they themselves recognize as inoffensive,” he says. There and elsewhere, most people prefer to kill them due to fear and loathing, although few of the species are venomous. In a 2014 study, Freitas reported that the Piraja’s lancehead (Bothrops pirajai) lives only in fragments of the Atlantic Forest in the southern part of the state of Bahia, and faces the same threats.

A broader view reveals a paradox: the most populated region of Brazil—from southern Minas Gerais State to the south of Santa Catarina State—has the greatest richness (number of species) and phylogenetic diversity (lineages) of snakes because of the variety of forms of vegetation and terrain. Most specimens were collected from this region, which facilitates the identification of new species. In a survey in the Paranapiacaba mountains, in the São Paulo metropolitan region, the biologist Vivan Trevine, of MZ-USP, found 16 species of snakes and 80 species of amphibians, a good sample of the diversity of wildlife throughout the state. There are also regions not yet properly explored by biologists that are rich in species and lineages, such as the forests and savannahs of the Parecis Plateau and the Ricardo Franco Mountains, in western Mato Grosso, and in the northern and central regions of the Andes (see maps).

Many years of silence
“We are collating information that has been collected over the last 250 years,” says Nogueira. In 1758 the botanist and zoologist Carl von Linné (Linnaeus) published one of the first descriptions of a Brazilian snake, a boa. “Studying how snakes are distributed in a region is a way to understand the formation and evolution of natural environments,” states Nogueira. “If we understand what led to the diversity of snakes, we may be able to conclude what happened in other groups of animals.”

on the facing page, a boa (larger snake) in a book published in Italy in 1864

Iconographie générale des ophidiens/Giorgio Jan and Ferdinando Sodelli … and a boa (larger snake) in a book published in Italy in 1864Iconographie générale des ophidiens/Giorgio Jan and Ferdinando Sodelli

The maps are being developed from about 100,000 specimen collection records, “all checked by at least one expert,” says Nogueira. It was a slow, meticulous task. Thais Guedes, of the Federal University of São Paulo (Unifesp), and Fausto Barbo, of USP, spent years examining the animals and identification tags contained in dozens of zoological collections in Brazil and abroad—she concentrated on animals of the scrubland and he focused on those of the Atlantic Forest. “There was a lot of information, but it was scattered, disorganized, and contained errors that had to be corrected,” says Ricardo Sawaya, of Unifesp. He and Barbo examined jararacas from the island of Santa Catarina in the Koenig Museum in Bonn, Germany, collected by the German zoologist Paul Müller between 1960 and 1970. Silently, the Butantan Institute technician Valdir José Germano has spent five years recovering information for studies like this from the remains of the snakes and their singed identification tags damaged by the fire that destroyed most of a collection of more than 80,000 samples at the Institute, in 2010.

Since 2012 the researchers have been providing information about the geographic distribution of species for the list of endangered species, published by ICMBio in November 2014. Otavio Marques, a Butantan biologist who has worked on the geographic distribution and natural history of species in the Atlantic Forest along the São Paulo coast for thirty years, commemorates the fact that the information on snakes and other groups of animals was used when preparing the guidelines for biodiversity conservation and recovery for the state of São Paulo, a document published in 2008 with the objective of recognizing and protecting areas with native vegetation with a high concentration of different animals and plants. “Conservation units have already been established in São Paulo based on these maps,” he says.

The snake islands
The island and forests of the Brazilian coast are proving to be a true nest of lanceheads: each location seems to have its own species, or at least unique varieties of a single species. Hundreds of golden lancehead vipers live in the trees of Queimada Grande Island—and only there. They are about 1 meter in length, with venom that allows them to kill small birds in seconds. Alcatrazes Island, about 30 km away, is home to hundreds of Alcatrazes lanceheads, about half a meter in length, which feed almost exclusively on centipedes. Now another species has been found, Bothrops otavioi, which eats toads and, so far, has only been found in one location, the forests of Vitória Island, in the Ilhabela archipelago-municipality. A candidate for a new species of jararaca lives on the neighboring island of Búzios and another lives, still anonymously, on an island further north, on the coast of the state of Espírito Santo.

For researchers, finding new species generates contradictory feelings, similar to the joy of someone arriving at a party followed by disappointment when they realize that the party is winding down. “We document the new species and, at the same time, classify them as endangered due to the high risk of loss of the native forests in which they live,” says Sawaya. He participated in the description of the jararaca on Vitória Island and worked on the characterization of the possible new species on neighboring Búzios Island, both inhabited by rustic fishermen’s families whose houses are encroaching on native forests.

The researchers believe that the coastal islands may harbor unique varieties of animals as a result of geographic isolation caused by the lowering of the sea level, a process that ended about 10,000 years ago and that may have favored the formation of new species. There is still be much to be discovered because “the state of São Paulo has more than 100 islands and Rio de Janeiro has more than 300, most with few biological surveys,” says Sawaya. It will probably not be easy to find the animals. “Snakes are an ungrateful animal to study; they are generally not easy to find,” notes Marques, “but on Queimada Grande you can see ten to fifteen jararacas a day. On Alcatrazes, five to ten a day.” An estimated two to three thousand jararacas live on each of these islands.

New snake species can be found even in urban forests. In 2014, researchers from São Paulo, Goiânia and Belém documented a new kind of coral snake, Micrurus potyguara, found in João Pessoa, Paraíba State. Based on Butantan Institute records from 2003 to 2007, Barbo found that 38 different species live in fragments of the Atlantic Forest in the municipality of São Paulo. The most frequent were another false coral, the sleep snake, an inoffensive slug-eating snake, and the venomous jararaca-da-mata, with a brown body and dark triangular markings.

Groundwork at the Butantan Institute: Valdir Germano rearranges the collection damaged by fire in 2010 and Selma Almeida Santos...

Eduardo CesarGroundwork at the Butantan Institute: Valdir Germano rearranges the collection damaged by fire in 2010 and Selma Almeida Santos…Eduardo Cesar

Discovery and loss
“If we do not act now, in 20 years there will be nothing to preserve,” warns Nogueira. “Many regions that I visited 15 years ago in Goiás, Mato Grosso and Bahia no longer exist; they are now being used for agriculture.” In 1997, while still a biology student in São Paulo, he went out to rescue animals for the first time in a region in the Cerrado that would be flooded by the Serra da Mesa hydroelectric plant being built in the northeast of the state of Goiás. Despite the skepticism of colleagues—the Cerrado is still seen as having poor biological diversity—Nogueira found “a stupendous wealth of lizards and snakes,” since it was a contact region between the Amazon forest and the plateau areas of central Brazil.

“It was what I called the paradox of the Serra da Mesa: we became aware of its diversity only when it was being destroyed. This also happened in other locations, and also with fish and other groups of animals,” he says. “We still depend on these events causing great destruction, like now in Belo Monte and Jirau, in the north of Brazil, to learn about the biological diversity of a region. Now we have the animals, identified and preserved in museums, but not the environments in which they lived. We need to carry out more planned biological inventories in intact areas such as parks and reserves, which are still almost unexplored.”

Biologist Hussam Zaher, a researcher and former director of the Museum of Zoology, experienced the same situation in 2014, after discovering a new genus and species of snake in the woods that will be flooded by another reservoir in the Amazon region. Another specimen of this snake was captured in another area, 150 kilometers away, which will also be flooded by a hydroelectric dam.

With his group, he works on the genetic and molecular analysis of 1,200 species of South American snakes in order to establish the origin and phylogeny—the family tree—of this group of animals. “Snakes are modified lizards that lost their legs as they evolved over the years, but we still do not know from which lizard groups snakes may have originated,” he says. Data analysis is expected to start in the first half of 2015. Preliminary results, with just 12 genes, indicated that the jararacas on the islands and on the continent are not different genetically and, therefore, could be the same species with morphological variations. “We are redoing the analyses with larger DNA samples,” states Zaher.

...  and Juliana Passos measure golden lancehead vipers bred in the laboratory

Eduardo Cesar… and Juliana Passos measure golden lancehead vipers bred in the laboratoryEduardo Cesar

Facing the military
Convincing people and the authorities of the need to preserve these animals is not easy. It is not enough to say that, without snakes, there would be more frogs and rats in the forests and cities. Nor that there are animals with unique habits, such as the Rhachidelus brazili, a black snake that eats only eggs and lives in the disappearing natural grasslands of the Cerrado, or that there are species that could represent a region—the red Caatinga lancehead (Bothrops erythromelas) “is the Caatinga embodied in a snake that lives only in low vegetation and at the foot of mountains,” says Nogueira.

The surgeon Rodrigo Souza, from the state of Minas Gerais, decided to act. He was moved by the decrease in native vegetation and killing of snakes by vehicles on roads in southern Bahia. In 2001 he bought a farm in Itacaré and founded a serpentarium to raise South American bushmasters (Lachesis muta), the largest venomous snake in the Americas, but seen less and less in the region. The snakes are kept in vivariums in a location surrounded by walls three meters high and 50 cm thick, to prevent the passage of armadillos, a requirement of environmental agencies. Souza, who works with researchers in São Paulo and Minas Gerais, announced the first reproduction of Atlantic Forest bushmasters in captivity in 2007. They had previously been classified as endangered.

In a meeting in Brasília at the start of 2013, Marques, from the Butantan Institute, asked Navy officials to stop carrying out shooting exercises on the rocks on Alcatrazes Island. The shooting, he argued, caused fires that could reduce the populations of jararacas and the Navy could be held responsible. “The officials agreed to stop exercises on Alcatrazes,” he recounts. In another meeting he used a utilitarian argument, asking which of the officials and politicians present suffered from hypertension. Seeing the arms raised, he reminded them that a widely used drug for hypertension, Captopril, was developed from the venom of the mainland jararaca (Bothrops jararaca).

Marques warned them that if the Alcatrazes species disappeared “we would lose a potential source of new drugs.” Since the venom of this species contains three specific proteins that differ from those found in the venom of the mainland jararaca, which feeds mostly on small mammals and not centipedes like the Alcatrazes lancehead, perhaps other drugs could be developed based on its venom.

The first specimens of the other island jararaca, the golden lancehead viper, arrived at the Butantan Institute in 1911, sent by Antonio Esperidião da Silva, who lived on Queimada Grande Island. Afrânio do Amaral, a researcher and one of the institute’s directors, was intrigued when he saw feathers in the feces of the snakes (at that time, no jaracara was known to eat birds) and visited the island several times. Then, a new problem emerged, the illegal commerce of snakes. “Some of our students received offers to bring animals back from Queimada Grande,” recounts Marques.

In 2010, with his team, he brought 20 snakes back from Queimada Grande and asked biologist Selma Almeida Santos to “take care of them as if they were your children.” Santos, with her team, studied sperm viability and the hormone cycle of the females to determine the best time to introduce pairs for breeding. The couplings were successful and 25 baby snakes were born. Four years later, the snakes are still kept in plastic boxes in one of the Butantan laboratories, but should be moved soon. “The next step is to release them in a wooded area so that they can live and reproduce without our assistance, and then repeat the process with other endangered species,” says Marques. “We have already brought in four Alcatrazes lanceheads.” In a few years he will know if the strategy paid off with this other island inhabitant and if it can be used to preserve other species that have not yet been lost.

Projects
1. Conservation biogeography of Brazilian snakes (No. 12/19858-2); Grant Mechanism: Post-doctoral research grant (Cristiano de Campos Nogueira); Principal investigator: Hussam El Dine Zaher (USP); Investment: R$249,800.70 (FAPESP).
2. Natural history of South American snakes: an evolutionary approach (No. 12/07334-9); Grant Mechanism: Regular Line of Research Project Award; Principal investigator: Otávio Augusto Vuolo Marques (Butantan Institute); Investment: R$295,631.75 (FAPESP).
3. Origin and evolution of snakes and their diversification in the neotropics: a multidisciplinary approach (No. 11/50206-9); Grant Mechanism: Thematic Project; Principal investigator: Hussam El Dine Zaher (USP); Investment: R$1,916,933.83 (FAPESP).

Scientific articles
FREITAS, M. A. et al. Biology and conservation status of Piraja’s lancehead snake Bothrops pirajai Amaral, 1923 (Serpentes: Viperidae), Brazil. Journal of Threatened Taxa. V. 6, No. 10, p. 6326-34. 2014.
FENKER, J. et al. Phylogenetic diversity, habitat loss and conservation in South American pitvipers (Crotalinae: Bothrops and Bothrocophias). Diversity and Distributions. V. 20, p. 1108-19, 2014.
GUEDES, T. B. et al. Biogeography, vicariance and conservation of snakes of the neglected and endangered Caatinga region, northeastern Brazil. Journal of Biogeography. V. 41, No. 5, p. 919-31, 2014.
SOUZA, R. C.G. Reproduction of the Atlantic Bushmaster (Lachesis muta rhombeata) for the first time in captivity. Bulletin of the Chicago Herpetological Society. V. 42, No. 3, p. 41-3. 2007.

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