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ECOLOGY

More uniform forests

Proliferation of native species resistant to environmental disturbances reduces biodiversity in the Atlantic Forest

058_061_FaunaFlora_203-1Karl F. P. Von Martius (Flora Brasiliensis)Plundered by fire and sword at the hands of humans for five centuries, the Atlantic Forest has reacted in whatever way it can in order to survive. A study conducted by scientists from Brazil and the United Kingdom who analyzed remnant fragments of tropical forest in northeastern Brazil suggests that environmental degradation due to human activities causes exaggerated propagation of a few tree species that are more resistant, at the expense of many other species. The result is an entire forest that is increasingly homogeneous—and impoverished—through a cascade of localized extinctions.

The effect is similar to what can be observed when an exotic invasive species colonizes a new environment. Without any natural enemies, the population of the new species proliferates quickly and eliminates native species that compete with it for the same environmental resources. “Specialists always fear the spread of exotic species, but we don’t have to wait for an invasion. A native species can perform the same ecological role as exotic species,” says Marcelo Tabarelli, a botanist at the Federal University of Pernambuco (UFPE). Tabarelli, along with Felipe Melo, also at UFPE, and Carlos Peres, an ecologist from the Brazilian state of Pará who is currently based at the University of East Anglia in the United Kingdom, have authored an article in the October 2012 issue of the journal Biological Conservation in which they describe the phenomenon of biotic homogenization caused by native species, which they call “winners.”

The winner-loser relationship in ecology was described for the first time in 1999 by American researchers Michael McKinney of the University of Tennessee and Julie Lockwood, then at the University of California at Santa Cruz. Their work described a catastrophic scenario for biodiversity in which a few species with a set of special characteristics—rapid growth, tolerance to environmental disturbances and ease of transport—colonized new ecosystems and caused homogenization. “McKinney was exploring the impacts of urbanization on species diversity, and I was working with invasive species,” recalls Lockwood, now a professor at Rutgers University in New Jersey. “Our initial conversations revealed a unifying theme of winners and losers.” But more important, she notes, was the fact that the success of some species under the new conditions did not appear to occur randomly. “I see this as a case of humanity pruning the tree of life,” Lockwood comments. “Some branches get cut, and others are left to grow, perhaps uncontrolled.”

Trumpet tree: embaúba, a rapid-growth species that is widely dispersed in disturbed areas of the Atlantic Forest

FABIO COLOMBINITrumpet tree: embaúba, a rapid-growth species that is widely dispersed in disturbed areas of the Atlantic ForestFABIO COLOMBINI

Their paper, however, only looked at the phenomenon as it applies to exotic invasive species. These globalized winners may in fact cause, and continue to cause, serious problems in insular ecosystems and at the higher latitudes. Continental tropical ecosystems, however, are practically immune to this type of invasion. “We have problems with exotic species in Brazil, of course, but we have native species that are much more successful and no one talks about that in the literature,” said Peres, as he passed through his native city of Belém in the state of Pará.

It may seem obvious to any careful observer that the Atlantic Forest—or any other forest that has been greatly impacted by human activity—loses diversity due to fragmentation. After all, starting along the edge of a degraded forest, fragmentation encourages the proliferation of tree species known as pioneers. They are the first species to spring up in a disturbed area because they like sunlight, have small seeds that are scattered by wind or small animals, they grow rapidly, are often small in size, and reproduce annually. Some of these characteristics—and not by chance—are shared with the exotic winners. Among the native species that do well in these conditions are pau-pombo or cupiúba (Tapirira guianensis), which has become one of the most common species in the Atlantic Forest, caboatã-de-leite (Thyrsodium spruceanum) and leiteiro (Hymatanthus phagedaenicus), a species whose density has increased more than 750% in the Northeast. Hardwoods and shade-tolerant trees that have slow growth, seeds scattered by large mammals and multiannual reproduction—such as virolas, sapucaias, Brazilian cherries and ucuúbas—succumb to the so-called edge effect. They are the losers in this process.

Regional scale
Evidence of homogenization on a regional scale, beyond small forest fragments, is still limited. One of the first papers to show the magnitude of the problem was published by Tabarelli’s group last year in the journal Diversity and Distributions. The Pernambuco-based researchers studied a 56,000-square kilometer region that stretches between the states of Alagoas and Rio Grande do Norte. They compared thousands of flora records in 12 areas of that macroregion in two time periods: from 1902 to 1980, when the expansion of sugarcane wiped out nearly the entire continuous forest in that area, and from 1981 to 2006, after the end of the expansion cycle promoted through Pro-Álcool, the National Alcohol Program.

The group discovered that, on average, flora throughout the northeastern Atlantic Forest were 28% more alike after 1980. “There was very rapid homogenization in a relatively short period, just decades,” Melo notes. “Now I go to Pernambuco and see something, and 300 kilometers farther up, in Rio Grande do Norte, I’ll observe something quite similar,” says Tabarelli, a native of the state of Rio Grande do Sul who has lived in Recife since the late 1990s. “That is inconceivable in undisturbed tropical forests.”

058_061_FaunaFlora_203-2Lobo, D. ET AL. 2011According to Lockwood, some of the resistance to invasive species exhibited by these biomes may occur precisely because there is so much diversity and each region is different. “The more native species, the less likelihood of open ecological niches that can be occupied by an exotic species,” the ecologist maintains. Homogenization could undermine the natural immunity of the ecosystem and create problems for Brazilian forests in the future. As South America’s economic importance grows and the area is increasingly included in international trade routes, the researcher stresses, it will be subject to greater exposure to invasive species brought aboard ships and planes. “I do not expect the pattern of resistance to invasive species to continue for long in places like Brazil and India,” she says.

Future risk of invasion, however, is the least of the problems introduced by native species proliferation. By replacing old, slow-growing forests with ones that are thinner and less diverse—which Tabarelli calls “capoeirization,” in reference to capoeira, the middle, shrubbery stage of secondary forest regeneration—such proliferation compromises a number of ecological functions, such as the capacity to host large animals, store carbon and control flooding along rivers. Crucial inter-species interactions, such as between large, seed-scattering animals and the trees that sustain them, are lost, and lead to localized or complete species extinction. One of the most famous victims of this process is the Alagoas Curassow (Mitu mitu), the most well-documented case of large-bird extinction in the Atlantic Forest, now found only in captivity.

Added to this vicious cycle is another pressure factor: hunting, which eliminates mainly large animals in forest fragments already impacted by the edge effect—the change in the structure of a forest that occurs along its margins due to greater exposure to wind and sun. As reported in a paper published last year in PLoS One, Peres and colleagues discovered that most of the Atlantic Forest in the Northeast is “disoccupied,” practically devoid of mammals larger than five kilos. The group examined 196 forest fragments in search of 18 species that had inhabited those areas (tapirs, spider monkeys, wild boars and jaguars) and found no more than four specimens at the same time in any fragment. In most of the places they visited, the residents had no memory of those animals existing in the region.

Global transformation
“This paper sheds light on a process of global change that is happening on a very large scale, and suggests that what we are seeing today in our backyard may be the “new normal,” says Lockwood, who, like McKinney, praised the Brazilians’ work.

The research, asserts Peres, has direct implications for Atlantic Forest conservation policy. “One of its messages is that it is important to preserve large, continuous stretches, because the edge effect in those areas is then less able to spread inward,” he says. “In this case, size does matter.”

The study’s findings reinforce the need for rigorous enforcement of the new Forestry Code, which will increase the risk of homogenization because of a reduction in the size of the strips of vegetation reserved as permanent preservation areas along riverbanks. The new law changes the way these strips are measured by calculating their width starting from the midpoint, rather than from the highest point during flood season, as the old law had mandated. And it calls for restoration of at least 15 meters on properties that have been cleared to the water’s edge—which is most of them. One can imagine at first that the restoration requirement will serve little purpose for restoring biodiversity in a forest already so affected by fragmentation and the edge effect. “That is a dangerous interpretation,” Peres maintains. “It’s like saying, ‘my uncle has hepatitis, so let’s go ahead and kill him,” he says by way of comparison. Even deteriorated fragments of the Atlantic Forest still provide services that a pasture or a farm do not offer.

“The Forestry Code will not enable forests to escape homogenization,” Tabarelli comments. He thinks that the 15- to 20-meter strip that the law will require farmers to reforest “is a large forest margin.” In the Northeast, however, even those strips are gone. “Regardless of the degree of homogenization, when it rains a little here, it floods the cities, and when it stops raining, there’s a water shortage.” Even though they may not solve the problem, the riparian forests that are to be renewed can help connect forest fragments that are presently condemned to die out as a result of the edge effect.

“Even a homogeneous fragment is extremely rich,” Tabarelli says. He believes that the best way to combat the problem of homogenization is to tailor forest restoration technologies to protection policies. He recalls that in São Paulo State, for example, the reforestation of the Atlantic Forest calls for planting at least 80 species. “They don’t have to abandon renewal; they need to make it more efficient.”

Now the group is beginning to look towards other regions for signs of homogenization induced by native species. Data from Peres and his colleagues suggest that this phenomenon also occurs in the Amazon’s Arc of Deforestation, though on a less destructive scale. The UFPE team is also partnering with researchers from the state of Paraíba and from Mexico to conduct large-scale comparisons. “It’s a phenomenon that still needs to be confirmed at other sites in order to have a sounder basis”, says Melo, “but it is expected, because there is a theoretical and empirical basis for it.”

Scientific articles
TABARELLI, M. et al. The ‘few winners and many losers’ paradigm revisited: Emerging prospects for tropical forest biodiversity. Biological Conservation. Oct. 2012.
CANALE, G.R. et al. Pervasive Defaunation of Forest Remnants in a Tropical Biodiversity Hotspot. PLoS One. 14 Aug. 2012.
LOBO, D. et al. Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Diversity and Distributions. v. 17. pp. 287-96. 2011.
CARDOSO DA SILVA, J. M. and TABARELLI, M. Tree species impoverishment and the future flora of the Atlantic Forest of northeast Brazil. Nature. v. 404 (6.773), pp. 72-4. 2000.
MCKINNEY, M.L. and LOCKWOOD, J.L. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology and Evolution. v. 14 (11), pp. 450-53. 1999.

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