Without the fruit of the juçara palm to eat
Without a strong branch to perch on
Without an environment to live in
The jacutinga awaits the end of all fauna.”
This verse, written in 1984 by Brazilian poet Carlos Drummond de Andrade, illustrates the process by which the wildlife in Brazil’s Atlantic Forest have lost their habitat and disappeared from the ecosystem over the years. The bird cited by Drummond is a good example.
The jacutinga, or black-fronted piping guan (Aburria jacutinga), is a turkey-size bird that occurs only in the Atlantic Forest. It once abounded throughout the sweep of the forest that hugs Brazil’s coast, from the state of Bahia in the east to Rio Grande do Sul in the south. But now it’s considered globally endangered, and in Minas Gerais, where Drummond was born, is critically endangered. In the state of Rio de Janeiro, where the poet lived most of his life, it’s likely extinct. Nationally, the jacutinga’s conservation status is listed as endangered on the red list maintained by ICMBio, the environment ministry’s administrative arm.
The victim of habitat destruction and degradation as well as uncontrolled hunting, the jacutinga presents a textbook example of how the Atlantic Forest’s loss of fauna, or defaunation, is unfolding. Local extinctions don’t just occur where the forest has disappeared; they also sometimes occur where the forest is still standing, the presence of trees masking the silence of an ecosystem in decline.
According to a survey conducted by the Fiquem Sabendo initiative, 48% of the threatened species in the Atlantic Forest are found nowhere else on Earth, including the jacutinga. In all, the biome hosts 1,160 plant species and 425 animal species categorized as threatened on the ICMBIO Red List.
Some are considered possibly extinct, including birds such as the kinglet calyptura (Calyptura cristata), last sighted in 1996; the Doxocopa zalmunna emperor butterfly, not seen in more than 60 years; the Campo Grande tree frog (Hypsiboas cymbalum), which disappeared more than 50 years ago; and the ituí-maraúna, or knifefish (Tembeassu marauna), which disappeared after the construction of a hydropower dam in its native river system.
These are only a few examples, all of them endemic species that evolved with the biome. There are also cases of species widely distributed throughout Brazil that have become rare in the Atlantic Forest or simply disappeared from some places. And while these may represent local extinctions, the result is the same: the actors disappear, and the show is lost.
Fernando Fernandez, a professor of ecology at the Federal University of Rio de Janeiro (UFRJ), says that, unlike deforestation, defaunation can’t be seen or measured by satellite images. “These are forests that no longer have large animals because they have been exterminated locally. There are no more tapirs, no more peccaries, no more collared peccaries, no more jaguars and so on. And this forest is silent,” he says. “A large part of the tropical forest is empty, and the overwhelming majority of Atlantic Forest areas are just like that; they are forests with no animals in them.”
This is the case in Tijuca National Park in Rio de Janeiro. At nearly 4,000 hectares (10,000 acres) and hemmed in by the urban sprawl of the metropolis, the park protects a forest massif that was largely replanted throughout the 19th century at the behest of Emperor Pedro II, Brazil’s last monarch. The pioneering reforestation work was motivated by the lack of water in what used to be of the Brazilian Empire and also by the elite’s demand for wooded spaces, according to the historian Warren Dean in his 1995 book With Broadax and Firebrand: The Destruction of the Brazilian Atlantic Coastal Forest.
With more than a century to grow and reestablish itself, the forest has returned to the Tijuca massif, which has been legally protected as a national park since 1961. With shady trees and a predominance of green, it presents a dazzling image of a healthy forest that has miraculously remained intact over time. But it’s not. The cycles of deforestation for logging and coffee farming, in addition to intensive hunting, have left scars that remain under the replanted canopy. The scars aren’t evident, precisely because they’re marked by absence: the original wildlife of the forest is no longer there.
“This is a conservation problem that tends to be underestimated, but it’s gigantic,” Fernandez says.
Today, humans are intervening in the forest again. But this time, rather than wiping out the wildlife, they’re trying to bring it back through Project Refauna — an initiative to reintroduce native species such as agouti rodents, tortoises and howler monkeys into Tijuca National Park.
Rotten fruit on the ground
The disappearance of wildlife compromises the health of the entire forest, as the animals play a crucial role in maintaining an ecological balance. Without them, countless natural interactions are lost. And it was precisely through a very unique rupture in the interaction that occurs in the Atlantic Forest, between the so-called agouti tree and agoutis themselves, that the empty forest issue emerged in Tijuca National Park.
The agouti tree (Joannesia princeps) is a large tree, growing 15-30 meters (50-100 feet) high. Its nuts measure up to 20 centimeters (8 inches), with two to three seeds each. When they fall to the ground, they’re consumed mainly by agoutis, a rodent the size of a domestic cat.
“Each day, ICMBio environmental analyst Ivandy Nascimento de Castro-Astor passed a row of agouti trees on her way to work, and she always saw the fruits on the ground,” says Alexandra Pires, scientific director of Project Refauna. “She began to wonder why she never saw an agouti, if there were so many agouti trees.”
Pires, who is also a professor at the Federal Rural University of Rio de Janeiro (UFFRJ), where she specializes in interactions between animals and plants, began looking into the mystery of the missing agoutis in 2006. At the time, she was researching the impact of forest fragmentation on palm trees, and realized that some species of palm trees stopped reproducing when agoutis weren’t around. “Because agoutis are major seed dispersers,” Pires says.
“That is the signature of empty forest: big fruit rotting on the ground,” Fernandez says. Fruit, he notes, is how plants reward animals for dispersing their seeds, and big trees need to have big fruits in order to have big seeds. That is, they depend on large animals. “If you have a bunch of fruit rotting on the ground, it’s because there’s something deeply wrong with that forest. It’s because all the big animals that should have been scattering those fruits are no longer there.”
This is particularly fatal in tropical forests, where studies estimate that between 70% and 90% of a region’s plant life may depend on its animal life at some point in the life cycle, mainly for reproduction.
A study by researchers from Project Refauna shows that Tijuca National Park has already lost two-thirds of its large and medium-sized vertebrates. “Of the 33 species that should be there, only 11 really do occur,” says study co-author Marcelo Rheingantz, a biologist at UFRJ. “Jaguars, tapirs, peccaries, collared peccaries, ocelots, oncillas, margays, ferrets, woolly spider monkeys, otters — they can no longer be found there. And they used to, they occurred at some point.”
Without seed dispersal, there are no new trees to replace the large old ones. A large tree usually lives for more than 100 years, which makes the consequences of an empty forest even more difficult to see, as they will likely be felt only after a few generations. “The big trees turn into what we call a forest of zombies,” Fernandez says.
Over time, the tendency is for the forest, empty of animals, to empty itself of its large trees as well and become a less dense forest dominated by plant species with small seeds, which are dispersed by the wind or by small animals, such as birds. “But the forest will also be doomed,” Fernandez says.
It was in light of this threat that Fernandez and Pires, together with Tijuca National Park biologist Castro-Astor, came up with the idea that culminated in Project Refauna in 2011, which was established as an NGO in October 2021.
Where did the agoutis go?
Agoutis (Dasyprocta spp.) are relatively common throughout Brazil, with 12 species occurring in the country. In Tijuca National Park, it’s the red-rumped agouti (Dasyprocta leporina).
By the early 2000s, agoutis had disappeared from the park. Possible factors for their local extinction included pressure from hunting both by humans and dogs, getting run over by vehicles, and fragmentation of the habitat. The fact that agoutis are active in the daytime may also have exacerbated the problem, making them easier prey for hunters and even a more likely to be roadkill, due to the heavy traffic on nearby roads during work hours.
Yet despite having disappeared from Tijuca National Park, agoutis can still be easily found elsewhere in Rio de Janeiro. In a part of the city known as Campo de Santana, a small urban park without major environmental attractions, agoutis are so abundant that they’re considered a pest. The agouti population of Campo de Santana is virtually all urban, which makes it the perfect source of animals for an ambitious project: reintroducing agoutis into the Tijuca forest.
Biologist Bruno Cid came up with the plan to reintroduce the agoutis in 2009, turning the mission into his master’s subject, with Fernandez and Pires as his advisers. To capture the agoutis, he needed authorization from the Parks and Gardens Foundation, which manages Campo de Santana, and had to go through a lot of red tape. Once he had them, he took the agoutis to Rio Zoo (now known as BioParque Rio), a partner in the project, so that veterinarians there could examine the animals and give medical and sanitary approval for their reintroduction into Tijuca. As the agoutis were quarantined, an enclosure was built that would allow them to begin adapting to their new environment in the park.
In 2010, the first eight agoutis were reintroduced into Tijuca National Park’s forest sector. The first population settled well, and the researchers soon found the animals feeding on the fruits or seeds of trees such as jackfruit, jaboticabeira, chichá, queen palm and, to everyone’s joy, the agouti tree. The main characteristic that makes the agouti a great seed disperser is its habit of hiding large seeds to eat them later. In the process of hoarding seeds in different places or stealing seeds hidden by other agoutis, they can spread them over distances of up to 300 m (nearly 1,000 ft) from where they were produced. Agoutis tend to eat seeds up to 1.5 cm (6 in) in diameter; anything larger gets buried, Pires says.
A few months after reintroduction, the researchers recorded the birth of three agoutis in the wild. In all, 31 individuals were reintroduced into the park’s forest sector. “The agoutis we reintroduced are no longer alive and the current population is larger than that initial number. One hundred percent of that population is made up of animals born in the wild,” Fernandez says. “This shows that there is a viable population, and that the agoutis are settled. Agoutis have been seen interacting with more than 40 different species of plants, consuming their fruit and dispersing their seeds.”
With that, one of the pieces of the puzzle was back in place, and the forest got one of its main seed dispersers back.
The idea of refaunation
The agouti experiment occurred around the same time that researchers led by U.S. biologist Josh Donlan published a paper proposing the return of the modern-day descendants of Pleistocene-era megafauna to the Americas. With animals such as mammoths, giant sloths and giant bison all extinct, the paper called for rewilding with elephants, lions and wild horses.
In response to the that 2006 paper, Fernandez and Luiz Gustavo Oliveira-Santos, at the time a colleague from UFRJ, wrote their own proposal. The Brazilian researchers’ article, published in 2010 in Conservation Biology, proposed an alternative conservation agenda to rewilding: refaunation. Rather than repopulate landscapes in the Americas with wildlife from Africa and Asia, they reasoned, why not bring back the native wildlife that had disappeared?
“We propose an alternative major conservation goal for the 21st century: refaunation through restoration of extant species to their original geographical distributions,” they wrote. “The world has plenty of empty forests in biodiversity-rich places where ecological interactions are waiting to be restored by the same species for which these interactions once evolved.”
“We are going to take these species that disappeared 50, 100 years ago, because, unlike the Pleistocene rewilding, they co-evolved with these forests,” Fernandez says. “So they wouldn’t be an evolutionary Frankenstein; they interact with a bunch of tree species that live longer than these animals, and those are the trees that are still there, waiting for someone to disperse their seeds and missing out someone that disperses their seeds.”
Thus was launched the concept of refaunation.
How to assemble a puzzle
In the Atlantic Forest, the list of large animals includes jaguars, pumas, collared peccaries, peccaries, tapirs, red brockets, primates such as howler monkeys and woolly spider monkeys, and large ground birds such as the red-knobbed curassow, black-fronted piping guan, and dusky-legged guan.
Reintroducing even a single species isn’t a simple process, and a number of criteria must be met to decide on the feasibility of bringing a long-lost animal back into its habitat.
“You need to think first about reintroducing the animals of low trophic levels,” Fernando Fernandez says. That is, the animals lower down the food chain: “If almost everyone is missing, as is the case of the Tijuca forest and many other places, many species are missing. So first you have to reintroduce the prey, and then you can bring the predators in. That’s crucial,” Fernandez says.
In addition to prioritizing prey species, it’s also important to bring back species that are generalists, Fernandez says. These are animals with a varied diet that adapt well to environments, without very specific needs, and that are generally more resistant.
After this come the animals that are strategically important to restore ecological processes that are essential for nature, such as seed dispersal and pollination.
Another important criterion is to select species that have large populations in captivity that are available for reintroduction. Taking individuals from a population that’s well-established in the wild to reintroduce them elsewhere may also be possible, Fernandez says, but this option requires even more care and study, so as not to cause imbalances in the source population.
Last but not least, animals that don’t cause too much conflict must be selected. “We are not going to put peccaries [Tayassu pecari] in the Tijuca forest, for example, because they form large groups, attack crops, and people kill them, even for food. So let’s not put peccaries, which won’t work out so close to a city and with so many people around,” Fernandez says.
The same goes for jaguars (Panthera onca), which, in addition to creating potential conflicts with the surrounding human population, have a typical range of 5,000 hectares (nearly 12,400 acres) — 25% larger than the total area of Tijuca National Park.
According to these criteria, the Project Refauna team made a list of suggestions for species reintroduction in the Atlantic Forest in general, and a more specific one for Tijuca National Park. In 2018, they brought together researchers, park and ICMBio officials and representatives of environmental agencies at a workshop to discuss and plan the priorities for the reintroduction in Tijuca, taking into account the reality of the protected area, surrounded by a heaving metropolis of 6.7 million people.
“There are many species that will not be able to return because the size of the forest will not support viable populations or because it could cause some kind of problem for local human communities,” Alexandra Pires says. “But we intend to bring back all we can, so that the forest really works like a forest, within its complexity and functionality. And what we always say is that Refauna’s point of view is to restore ecological processes. Because several of these species that we reintroduce are not threatened fauna, they are not rare animals, but they need to be there for some processes to take place.”
The species reintroductions planned for Tijuca National Park started with the agouti, a relatively resistant prey and an excellent seed disperser.
The second species on the list, according to the criteria, was the howler monkey (Alouatta guariba), a large, resistant and very versatile primate. It eats more leaves than fruit, which means there’s abundant and easy food for it in Tijuca. It’s also a charismatic animal, which helps draw attention and raise people’s awareness about the project.
The reintroduction of howler monkeys began in 2015, when six individuals from the Rio de Janeiro Primatology Center (CPRJ) were released in the park. Two of them had to be removed later because they were interacting with visitors — a behavior considered problematic to preserve the animals’ wild nature — while one female died, and one male left the group and escaped the researchers’ monitoring. In the end, only one couple remained, but they’ve had five offspring so far.
In 2017, the park’s primates were threatened by an outbreak of yellow fever, a virtually fatal disease for howler monkeys, which have about a 90% chance of dying if infected. While the disease didn’t kill any of the howler monkeys in the project, it served as an important warning to the researchers, who suspended further releases. With the development of a vaccine for primates against yellow fever in 2020, the procedure for reintroduction of howler monkeys started to include a vaccination step.
A new group of howler monkeys is now awaiting immunization before it can be taken to the forest. The next new release is are expected in the first half of 2022.
The last species on Project Refauna’s reintroduction list for the Tijuca forest is the yellow-footed tortoise (Chelonoidis denticulata), or Brazilian giant tortoise, which is a resistant animal and an excellent seed disperser.
The species is thought to have gone locally extinct 200 to 300 years ago. Releases began in 2020, with 50 individuals reintroduced so far. The group has already suffered some losses, including encounters with dogs, and today the park’s tortoise population is 41.
A great disperser of seeds that require the process of chemical reaction that comes with passing through the digestive tract, yellow-footed tortoises can disperse large seeds over a wider area than agoutis. “The acid in the stomach of the tortoise, which takes four or five days to digest what it eats, triggers germination,” Pires says.
“We are trying to build it from the bottom up,” Fernandez adds. “Later on, we can try to place medium-size predators.” Among the species most conspicuous by their absence from the Tijuca massif are the carnivores. Today, only three carnivore species still occur in the park: the ring-tailed coati (Nasua nasua), the crab-eating racoon (Procyon cancrivorus), and the crab-eating fox (Cerdocyon thous). “A very promising species, for example, is the ocelot [Leopardus pardalis],” Fernandez says. “It is a 15-kilogram [33-pound] cat. And it has the smallest home range of all the Neotropical felids. So it would be possible to consider placing a population of ocelots in the Tijuca forest.”
The possible return of the ocelot or other predators depends, among other things, on the establishment of a rich variety of available prey, such as agoutis, pacas and other rodents and marsupials.
The road to filling an empty forest with life is a long one, and each step requires robust planning and lots of monitoring.
Reintroducing a species takes several steps, such as defining where the animals will come from, when and how they will be transported, the release protocol, how monitoring will be carried out, what type of trackers to use, down to the more mundane process of obtaining licenses.
In this sense, Tijuca National Park works as a perfect laboratory. Isolated from other natural areas, any possible imbalance can be quickly identified and addressed. Refaunation isn’t a simple science, but rather a necessary path for ecological restoration of historically degraded environments.
“Monitoring helps us because we can still take action, we can always reassess and carry out adequate management; it’s adaptive management, as we call it,” Pires says. “We reanalyze and see what kind of management we have to do for that population.”
Ongoing research also helps to measure the impact of reintroductions on the plant life, including the effect of the return of seed dispersers on forest dynamics. While forest dynamics play out in slow motion, the Project Refauna team has already managed to document interactions. “For Astrocaryum aculeatissimum [the brejaúva palm] and for the agouti tree, we proved that there is more restoration, recruitment, germination where these animals [agoutis and tortoises] are present,” Pires says.
The impacts of howler monkeys are also being measured. The species has already been observed interacting with more than 60 plant species, in addition to a particular, and very important, interaction with more than 20 species of dung beetles — an essential insect for ecological dynamics, including seed dispersal and soil fertilization and aeration.
The next reintroductions
Discussions about the reintroduction puzzle aren’t simple and depend on a number of factors. The Project Refauna team is already working with the real perspective of reintroducing blue-and-yellow macaws (Ara ararauna) in the park. These large birds with powerful beaks are great dispersers that can travel long distances with the seeds, a feature that distinguishes them from other dispersers. In addition, their beauty and charismatic aspect can help change the way park visitors relate to them and make people aware of the importance of native fauna and nature conservation.
However, before the macaws return to add some color to Rio de Janeiro’s skies, the Project Refauna team underscores the need for awareness-raising work with the surrounding communities, due to the risk of the macaws being captured for the pet trade or interacting — unhealthily — with humans, who may want to feed or touch the animals.
Also a hypothetical candidate for reintroduction is the green iguana (Iguana iguana). The feasibility of this is being studied by a professor from Rio’s West Zone State University (UEZO) who works with Project Refauna.
“We are also thinking about maybe reintroducing hawks and snakes, because these species could play the role of predators, controlling prey populations, so that the community can achieve greater stability,” says Marcelo Rheingantz, the UFRJ biologist. “Because today we have that apparent forest, but we lack the actors in the show.”
Restoration is a must
Reintroducing native animals is a major management intervention. There are other strategies for bringing fauna back to an empty forest. One of them is to establish ecological corridors between natural areas that allow animals to reoccupy those places naturally.
In the case of Tijuca National Park, however, that’s not a viable option. The park’s forest sector is nearly 10 kilometers (6 miles) from Pedra Branca State Park, which is considerably bigger and has a larger wildlife population. Between the two, however, lie insurmountable barriers such as four urban neighborhoods and two express bus routes, in addition to the busy Grajaú-Jacarepaguá road.
“The Tijuca forest is perhaps the extreme example of defaunation, of an empty forest,” Rheingantz says. “And the species will not come back because there is an urban area in the middle of the road, a city of over 6 million people. Agoutis will not leave Campo de Santana, stroll along Presidente Vargas Avenue, climb the mountains in Alto da Boa Vista and arrive at the forest. They just won’t. We have to take them there, then reintroduction is justified, because reintroduction is a management tool.”
In the Atlantic Forest as a whole, however, the forest restoration strategy and the creation of corridors can help reduce the problem of empty forests. “Between 15 and 28% of what used to be the Atlantic Forest remains. And 80% of those remaining areas are fragments under 50 hectares [124 acres],” Rheingantz says. “In other words, we cannot think of placing many species in these very small fragments. And the few large areas that remain generally have much more diverse communities but still lack some important elements.
“First we started locally, in Tijuca [Forest], then we expanded to the Guapiaçu Ecological Reserve, and then we realized that we needed to do broader work, in the sense of thinking of the Atlantic Forest as a landscape unit, and thinking about using these larger fragments, and reconnecting them,” he adds.
For this broader plan, the jaguar has become the reference in terms of refaunation, as the largest predator in the Atlantic Forest and the one that needs the largest area to survive. “When we think about jaguars, we have to think about these large areas that still remain and how jaguars will naturally return to the areas where they can still live,” Rheingantz says.
According to a study being carried out by the researchers, there are 15 to 25 areas in the Atlantic Forest where jaguars could live, called refaunation units. In addition to jaguars, there are two other key species, peccaries and tapirs, that aren’t present in many of these areas and that constitute the jaguar’s main prey.
In the Atlantic Forest, where about three-quarters of the biome has been destroyed, it’s essential to reconnect forest fragments to ensure that the actors of the show get their stage back. There is no refaunation without restoration, and vice versa.
Jansen, P. A., Hirsch, B. T., Emsens, W., Zamora-Gutierrez, V., Wikelski, M., & Kays, R. (2012). Thieving rodents as substitute dispersers of megafaunal seeds. Proceedings of the National Academy of Sciences, 109(31), 12610-12615. doi:10.1073/pnas.1205184109
Genes, L., Cid, B., Fernandez, F. A., & Pires, A. S. (2017). Credit of ecological interactions: A new conceptual framework to support conservation in a defaunated world. Ecology and Evolution, 7(6), 1892-1897. doi:10.1002/ece3.2746
Josh Donlan, C., Berger, J., Bock, C., Bock, J., Burney, D., Estes, J., … Greene, H. (2006). Pleistocene Rewilding: An optimistic agenda for twenty‐first century conservation. The American Naturalist, 168(5), 660-681. doi:10.1086/508027
Oliveira-Santos, L. G., & Fernandez, F. A. (2010). Pleistocene rewilding, Frankenstein ecosystems, and an alternative conservation agenda. Conservation Biology, 24(1), 4-5. doi:10.1111/j.1523-1739.2009.01379.x
* Published in english by Mongabay. Translated by Roberto Cataldo.
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