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ECOLOGY

Forests without animals

Decline of animal populations poses as serious a problem as deforestation

Amphibians like the chocolatefoot leaf frog Phasmahyla cochranae are highly sensitive to environmental changes

CÉLIO HADDAD/UNESPAmphibians like the chocolatefoot leaf frog Phasmahyla cochranae are highly sensitive to environmental changesCÉLIO HADDAD/UNESP

The annual release of data on deforestation is crucial for assessing the threat to forest biomes, but the data provide an incomplete picture of the situation. Even in areas that have not been deforested, defaunation—the term describing a marked decline in animal populations—is occurring at a rapid rate, posing a problem as significant and hard to control as deforestation, according to a paper published in the journal Science in July 2014.

The research was coordinated by Mexican biologist Rodolfo Dirzo of Stanford University, and the coauthors of the paper include Mauro Galetti of the Ecology Department at São Paulo State University (Unesp) in Rio Claro, a long-time collaborator with the Stanford team. The review in Science reinforces what Galetti and his colleagues in Brazil have shown in recent years, especially in the Atlantic Forest: the increasing depletion of the fauna in these ecosystems. “These areas are not deforested, but they have been depleted of animals, initially because of pressure from hunting that continues to this day, but also due to a number of other factors such as cutting down juçara palms, which are a major food source for animals,” Galetti says. Dirzo’s group estimates that, on average, vertebrate species worldwide have lost almost a third of their population since the 1970s. Some vertebrates are more severely affected; over 40% of amphibian species, for example, are considered to be endangered, compared to 17% of bird species.

It is only natural that the decline in vertebrates is being watched more closely by both researchers and the public. To begin with, vertebrates are more visible than most invertebrates, and many of them are considered charismatic species that become widely known because of their featured roles in conservation campaigns. The survey published in Science, however, also assembled available data on invertebrates and concluded that the situation for these animals is also cause for concern.

About two-thirds of the monitored invertebrates have lost an average of 45% of their population. “The fact is that we need more data, but I don’t think that figure is an exaggeration,” Galetti says. “What is happening is that these declines generally refer to invertebrates that used to be very abundant, and consequently they were monitored in field research. The scenario would probably be worse if naturally rarer species were included in the calculation.”

Tapirs, the largest herbivores in the Atlantic Forest, are important agents of seed dispersal

FÁBIO COLOMBINITapirs, the largest herbivores in the Atlantic Forest, are important agents of seed dispersalFÁBIO COLOMBINI

Domino effect
In addition to the more obvious consequences of a scarcity of animals such as the risk of extinction, defaunation raises concern because it can trigger a series of ecological domino effects: the loss of key species tends to affect various other animals and plants, causing repercussions that can jeopardize both the normal functioning of an ecosystem and the environmental services it provides to humans, such as soil fertility or the abundance of drinking water.

The effect is more obvious with predators at the top of the food chain, such as jaguars. Their presence prevents smaller predators from dominating the other animals, and the result is a greater diversity of those feline “subjects”.

Medium and large-bodied herbivores, in turn, are the principal dispersers of seeds from large fruits (tapirs are very skilled at that role), and they also act as “architects,” opening up clearings and beating down young plants. Even the abundance of amphibians depends to some extent on large herbivores that trample the ground along the edges of streams, thereby creating depressions where frogs and toads may find shelter.

Regardless of the type of animal, however, the situation in the Atlantic Forest does not appear to be very favorable. In a paper published in the July 2013 issue of Biological Conservation, Galetti and colleagues mapped the situation of four of that biome’s iconic species: the largest predator (jaguar), the largest herbivore (tapir), the largest seed eater (white-lipped peccary) and the largest arboreal seed disperser (woolly spider monkey, the largest monkey in the Americas). After analyzing data from nearly 100 different locations, they concluded that 88% of the remaining Atlantic Forest is completely depleted of all four of these species, and 96% is depleted of at least one of them. And worst of all, the Unesp group notes, less than 20% of the remaining forest fragments would be a suitable habitat for all four of these key species.

An analysis of a broader range of medium and large-bodied species shows little improvement in the situation. In a 2012 study published in PLOS One, a team including Gustavo Canale of Mato Grosso State University (UNEMAT) and Carlos Peres of the University of East Anglia in the U.K., assessed the presence of 18 species of mammals (including the aforementioned species as well as tamanduas, armadillos, howler monkeys and others) in nearly 200 Atlantic Forest fragments stretching over three Brazilian states (Minas Gerais, Bahia and Sergipe). They found that an average of only four of the 18 species still persist in fragments of up to 5,000 hectares. Even in larger patches of forest, only seven species are likely to share the environment.

Large monkey species such as howler monkeys have disappeared from some areas due to overhunting

RAIMUNDO PACCÓ / FOLHAPRESSLarge monkey species such as howler monkeys have disappeared from some areas due to overhuntingRAIMUNDO PACCÓ / FOLHAPRESS

In the few places where these animals still exist, biologists fear that males and females may have difficulty finding partners. The population decline may also increase the risk of crossbreeding between close relatives, creating offspring with congenital problems or low resistance to disease. The available data on jaguars in the biome suggest such a scenario, says geneticist Eduardo Eizirik of Pontifical Catholic University of Rio Grande do Sul. “There is clearly a reduction in diversity, and the fragments are also becoming differentiated from one another, probably as a result of intense genetic drift [random loss of variation],” he says (see Pesquisa FAPESP Issue No. 215).

Big little changes
For invertebrates and small vertebrates, the ecological damage from defaunation is clear. One example is the role of insects as pollinators, in particular the many species of bees; it is no coincidence that worldwide colony collapse has been a source of concern for farmers.

In the case of amphibians, which are very vulnerable to environmental disturbances, there are records of dramatic population declines in regions such as the Andes and Central America. In these instances, there may be two factors at work in a perverse synergy: climate change that warms the cool, moist environments preferred by amphibians, and the Batrachochytrium dendrobatidis fungus, which occurs in these conditions and can cause many of these species to disappear.

Much of the remaining amphibian diversity in the Atlantic Forest is concentrated in mountainous and relatively cooler areas, where B. dendrobatidis has been identified in the past decade, leading experts to fear a repetition of the Andean scenario. For now, however, the situation is turning out to be more complex, according to zoologist Vanessa Kruth Verdade of the Federal University of the ABC.

“The findings indicate that each species responds differently to climate change. Moreover, it was discovered that the strain of the fungus in Brazil is old, prior to the declines, which raises questions about its significance as a cause of the declines within the national territory,” she explains. Although there are data on population losses for several amphibian species in Brazil, assessing the extent of the problem and understanding its causes still pose a challenge due to the absence of historical data on these populations and a lack of knowledge about their natural variation, says Verdade. Be that as it may, what is certain is that defaunation eventually strengthens the vicious circle of forest depletion. “It has a negative feedback effect on the system by weakening the arboreal vegetation as a consequence of the breakdown of ecological communities,” she says.

A clear example of this phenomenon can be seen in a strange group of invertebrates, popularly known as dung beetles. As the name suggests, they eat feces and use the excrement produced by large mammals for their nests. In another paper published in Biological Conservation in 2013, Galetti and his colleagues showed that, in defaunated areas of the Atlantic Forest, a series of changes are affecting dung beetles: the species diversity of these insects is shrinking, as is the size of the beetles, while the absolute number of individuals is increasing. This is not just a curiosity, because these changes can have a considerable impact on the way in which organic matter is recycled in the forest soil, consequently affecting plant growth and a variety of other parameters.

Rebuilding communities
In Galetti’s view, these findings make it clear that there is a need to rethink environmental recovery efforts. “There are currently many projects designed to create ecological corridors through tree-planting, but restoration of the fauna, though much more difficult, is essential,” he explains.

The first and most obvious step is to enforce hunting bans, he points out, but it may be equally important to consider reintroducing animals with an eye to the ecological role each of them plays in the biome. “Projects are conceptualized in terms of the threat to that particular species. Depending on the situation, however, another species might be equally attractive. It is clearly important to recover the population of golden lion tamarins, but in some cases, reintroducing a different fruit eater may have the same effect,” he says by way of comparison. In other words, might there be “ecological packages” of, for instance, a large-bodied herbivore, a medium-sized one, and small and large predators? “Yes, but this would have to be done one step at a time—the herbivores first, for example, and then the carnivores. It’s a slow-going process of refaunation that we will have to undertake.”

Project
Effects of the defaunation gradient on plant herbivory, seed predation and dispersal: The Atlantic Rainforest perspective (No. 2007/03392-6); Principal investigator Mauro Galetti (Unesp); Grant mechanism Thematic Project; Investment R$692,437.03 (FAPESP).

Scientific articles
DIRZO, R. et al. Defaunation in the anthropocene. Science. v. 345, n. 6195, p. 401-06, 25 jul. 2014.
CULOT, L. et al. Selective defaunation affects dung beetle communities in continuous Atlantic rainforest. Biological Conservation. v. 163, p. 79-89. jul. 2013.
JORGE, M. L. S. P. et al. Mammal defaunation as surrogate of trophic cascades in a biodiversity hotspot. Biological Conservation. v. 163, p. 49-57. jul. 2013.
CANALE, G. et al. Pervasive defaunation of forest remnants in a tropical biodiversity hotspot. PLoS One, v. 7, n. 8, e41671. 14 ago. 2012.

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