Their findings confirm the answer to one of ecology's oldest and thorniest questions: why is the world green? It also seems to put to rest a competing theory that plants protect themselves from herbivores through physical and chemical defenses.
The researchers drew their conclusions from study of a Venezuelan valley flooded 20 years ago by a hydroelectric project.
The research, reported in the March 2006 issue of the British Ecological Society's Journal of Ecology, was supported by the National Science Foundation. The paper was co-authored by Terborgh, Kenneth Feeley and Bradley Balukjian from Harvard University, Miles Silman from Wake Forest University, and Percy Nuñez of Universidad Nacional "San Antonio de Abad" de Cusco in Peru.
Their results support the so-called "green world hypothesis," first proposed in 1960 by United States scientists Nelson Hairston, Frederick Smith and Lawrence Slobodkin. Despite being almost 50 years old, the green world hypothesis has been almost impossible to test until now.
"Since the landmark paper by Hairston et al, ecologists have been debating whether herbivores are limited by plant defenses or by predators," wrote the authors. "The matter is trivially simple in principle, but in practice the challenge of experimentally creating predator-free environments in which herbivores can increase without constraint has proven almost insurmountable."
However, the researchers realized that the hypothesis could be tested on a vast hydroelectric project.
Within Venezuela's Caroni Valley, an area of 4,300 square kilometres was flooded in 1986 to create a lake (Lago Guri) containing hundreds of islands that were formerly fragments of a continuous landscape.
Terborgh and his team monitored the vegetation at 14 sites of differing size. Nine of the sites were on predator-free islands, while the others were on the mainland or on islands with a complete or nearly complete suite of predators.
They found that, by 1997, small sapling densities on small islands were only 37 percent of those of large land masses and by 2002 this had fallen to just 25 percent. Most of the vertebrates present in regional dry forest ecosystem had disappeared from small islands, including fruit eaters and predators of vertebrates, leaving a hyperabundance of generalist herbivores such as iguanas, howler monkeys and leaf-cutter ants.
"Mere numbers do not do justice to the bizarre condition of herbivore-impacted islets," the authors wrote. "The understory is almost free of foliage, so that a person standing in the interior sees light streaming in from the edge around the entire perimeter. There is almost no leaf litter, and the ground is bright red from the subsoil brought to the surface by leaf-cutter ants.
"Dead twigs, branches and vine stems from canopy dieback litter the ground, and in places lie in heaps. But in striking contrast with this scenario of destruction, the medium islands presented a relatively normal appearance."
Besides proving that the green world hypothesis is correct, Terborgh's team's results have important implications for the debate raging in many countries over reintroduction of top predators such as wolves. "The take-home message is clear: the presence of a viable carnivore guild is fundamental to maintaining biodiversity," the authors wrote.
Information collected for the Journal of Ecology report is a five-year update of results published by Terborgh and 10 other scientists in the Nov. 30, 2001, issue of the journal Science.
"The Science article reported on the first plant census we did, involving 15,000 plants, but it only gave us a snapshot in time," Terborgh said in an interview. "We could see that there were huge differences between the little islands that didn't have any predators on them, and larger islands that did have predators. But we couldn't say much about where that was going to go in the future.
"This article reports on the re-census," he added. "Indeed, during that five-year interval the populations of small, sapling-level plants continued to decline quite radically. And there's no question that the vegetation on these islands is just in a state of collapse."
A drought that began in 2001 and reached extreme levels in 2003 has now ended the study, Terborgh reported.
"By 2003, the lake level had dropped 26 meters," he said. "By then, I think only three of the islands were left surrounded by water. That ended the experiment because it allowed the animals to redistribute themselves in their own fashion. The overcrowded populations of the plant-eating animals that had been the object of our studies simply dispersed.
"The fundamental premise of the whole project was our ability to study predator-free space, and that condition was no longer met. In one period in 2003 we found six different predators on islands that previously had no predators."