The empty forest

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Science  25 Jul 2014:
Vol. 345, Issue 6195, pp. 396-399
DOI: 10.1126/science.345.6195.396

A beleaguered national park in Borneo hints at what can happen when animals disappear.

Darkness comes quickly at Lambir Hills National Park in western Borneo. The cicadas fall silent, and tree frogs start to chirp softly. Tourists and day hikers have left the ancient forest, so it is a good time to look for the slow loris, a shy arboreal primate. But one night, while ecologist Rhett Harrison was searching for wildlife, a man stepped out of the shadows. The hunter scowled; he knew he wasn't allowed to shoot the animals in the park. No one spoke. The man raised his bakakuk, a homemade shotgun. Unarmed and helpless, Harrison slowly backed away.

The encounter was a rare, heart-stopping event in several years of research at the park in the mid-1990s. Usually, Harrison only heard distant gunshots echoing through the forest or came across snares. But the cost of the hunting became clear with time. In Lambir—one of the most diverse forests in the world—the richness of animals has declined precipitously over the last 3 decades, work by Harrison and others has shown. Flying foxes, sun bears, gibbons, rhinoceros hornbills. All gone. “It's empty of large wildlife,” says Richard Corlett of the Xishuangbanna Tropical Botanical Garden in Menglun, China. “There's been dramatic and rapid change.”

A suspension bridge helps researchers study changes to the forest in Lambir Hills National Park.


Lambir is not alone in its defaunation, a process in which an ecosystem loses animals. Much of Asia, Africa, and Latin America also suffers from poaching and overhunting. In some places, the quarry are elephants, tigers, or other high-value species for the international black market. Elsewhere, hunters are just trying to put meat on the dinner table. “It's an epidemic that's going through tropical forest reserves,” says Harrison, who works for the World Agroforestry Centre in Kunming, China.

In 1992, Kent Redford, then of the University of Florida, brought widespread attention to the potential fallout from this epidemic, arguing that the forest itself could not survive without the animals that help plants reproduce. “We must not let a forest full of trees fool us into believing that all is well,” he wrote in BioScience. “An empty forest is a doomed forest.”

Since then, researchers have been documenting animal losses and their consequences for a wide range of species and ecosystems including pollinators in farm fields and sharks on coral reefs. Lambir is a key case study. Long-term research on its vegetation is revealing how a forest changes when it loses the herbivores that once thinned saplings and the fruit eaters that dispersed seeds. Borneo is also the scene of more hopeful developments, as researchers and nongovernmental organizations seek ways to stem the damage. “Overhunting is bad for both people and wildlife,” says Jedediah Brodie of the University of British Columbia, Vancouver, in Canada. “If we can make hunting sustainable, then it's a win-win.”

Deer and pigs are primary targets of hunters looking for meat to sell or eat.


What is not sustainable is the millions of metric tons of meat harvested in central Africa and the Amazon each year, or the impact of China's burgeoning demand for bear gallbladders and other animal parts used in traditional medicine. In the forests of Laos and Vietnam, few animals heavier than 80 grams can now be found. “There is deafening silence,” says Carlos Peres of the University of East Anglia in Norwich, U.K.

Researchers exploring the impacts of defaunation consistently find that it favors plants with wind-dispersed seeds over those that rely on animals to disperse their seeds. In Panama, S. Joseph Wright of the Smithsonian Tropical Research Institute and colleagues have linked hunting to an increase in woody vines called lianas, which cast their seeds into the wind. Other studies in Peru, Thailand, and Nigeria have also shown changing patterns of plant distributions. But long-term studies in Lambir offered researchers a closer look at what happens to a forest as ever more animals disappear.

While some researchers study insects in the park, others have probed the fate of plants based on their fruit or seed.


BORNEO'S INDIGENOUS NOMADS, the Penan, long made a living by hunting, but their impact was minimal. They would move their forest camps when the sago palm became scarce and game, as they put it, turned shy. In addition, their communities were small relative to the forest.

Life for the Penan and other peoples began to change rapidly in the 1970s. Loggers carved roads into previously isolated areas, making it easier for outsiders and migrants to hunt deep in the forest. They would take game back to village markets or sell it to the work camps. Although the Indonesian government had long since banned guns, dangerous homemade shotguns proliferated. Even more devastating has been the use of snares, which indiscriminately kill animals.


Yet well into the 1980s, Lambir (established in 1975) was reachable only by a dirt logging road. It would wash out in the rainy season, giving the park some protection. Helmeted hornbills filled the sky with the whoosh of their wings. Hunters covet these magnificent birds, because artisans carve the casque, a large, ivorylike protrusion on its upper beak. “It was as near to an undisturbed forest you could have had at that time,” Harrison says.

Now, after decades of logging, the park is a lonely island in a sea of oil palm plantations. The road to the park was paved in 1987, easing access by tourists and nearby residents of Miri, the center of Borneo's petroleum industry. Its 6952 hectares contain waterfalls and sparkling pools. The trees growing on the clay soil are gargantuan, dwarfing those of the Amazon. “It's like being in a gothic cathedral,” says Peter Ashton, a retired botanist who set up research plots there in 1964. The warm, moist air, smelling a bit like cigars, buzzes with insects. To many, especially newcomers, the park looks pristine.

But the forest is not what it was. The helmeted hornbill was long gone by the time Harrison arrived in 1994 to start his doctoral research on fig trees. And other species, such as the swan-sized rhinoceros hornbill and the gibbon, seemed rarer than they should have been. “I felt there was something wrong,” Harrison recalls. It wasn't a big leap to suspect hunting. In addition to hearing the blasts of shotguns, he came across snares and evidence of hunters' camps.

In the evening, when Harrison and his colleagues drove to Miri, they would sometimes see sport hunters parked in large four-wheel-drive vehicles, shining spotlights into the forest to catch reflections of wild eyes. In the city, curio shops sold earrings made from hornbill casques. Vendors in the open-air market hawked small mammals in cages, ready to be cooked or taken home as pets.

Years later, Harrison decided to pull together the data about the decline in animal species. He went through previous records, interviewed older researchers, and walked his own surveys. The situation appeared grim: A camera-trap survey in 2004 detected only one bearded pig in 8 months. And when Harrison spent 6 months in the park in 2007, he couldn't find a single animal that weighed more than a kilogram. Not all animals are gone; small birds, rodents, and geckos persist, for example.

Harrison decided to explore the consequences of these losses, taking advantage of the data that the Smithsonian has collected at Lambir since 1991. Every 5 years, researchers and staff members spend about 9 months measuring each and every one of the 370,000 trees and saplings in a 52-hectare plot. Harrison and colleagues pored over books and museum records to figure out how these trees disperse their seeds. Then they analyzed how common each species was across the plant surveys.

Orangutans and rhinoceros hornbills are gone from Lambir, leaving only small creatures such as geckos.


The changes were dramatic. For all species, they found that the density of the saplings had increased by 25%, likely from the paucity of deer and other herbivores that thin new growth. The higher density of saplings could be a problem, as overcrowding can promote the spread of plant diseases. Even though there were more saplings, their diversity has fallen by 1.9% since 1992, they reported online in March 2013 in Ecology Letters.

This is large and rapid change for a rainforest, Harrison says, and it's due to the loss of seed dispersal by animals. Another impact: Compared with wind-dispersed species, saplings of fruit trees became more clustered around the adults, especially tightly so for species with large fruit. Eventually, the distribution of adult trees may shift, and some species could disappear.

A FIRM CONCLUSION ABOUT THE FATE of the forest is still elusive, as much is unknown about the demography of trees. “It can be overwhelming to go into a rainforest and try to understand anything,” Brodie says. “There's just so much going on.” Even Redford, who in 2011 established Archipelago Consulting in Portland, Maine, doesn't want to oversell the risk. “It's my suspicion that there is a lot more hype than data about how everything goes to hell once the big animals are gone,” he says. It could be that small, reclusive animals will take over the role of dispersing seeds, for example.

Lisa Curran of Stanford University, an anthropologist who studies land use change and biodiversity in Borneo, even questions how big a role hunting has played in Lambir's loss of fauna. The park may be simply too small to support many large animals, she says. And because it's surrounded by plantations, animals emigrating from other areas can't easily replenish the population.

Some officials and activists in various parts of Borneo are nevertheless taking action against overhunting and illegal trade, with mixed success. Enforcing hunting bans can be a challenge. This past December, wildlife rangers raided an open-air market in the state of Sabah. They confiscated 160 kilograms of unlicensed meat from sambar and barking deer. Angry villagers then hurled stones and machetes, damaging vehicles and injuring an officer. Many conservation groups shy away from confronting overhunting, because they don't want to be seen as hurting local livelihoods.

But some groups are helping head off poaching and illegal logging. For example, staff with the HUTAN-Kinabatangan Orang-utan Conservation Project patrol part of a 26,000-hectare wildlife sanctuary in northeast Borneo. And some local communities have stepped up as well. Sungai Wain Protection Forest, an upland reserve on the east side of Borneo, was protected after the nearby city of Balikpapan realized its importance for providing water for the local petroleum refinery. It retains abundant wildlife, including many rare birds and mammals. “You don't need a really great forest,” Harrison says. “What you need is protection from hunting.”

As for Lambir, many think the outlook is gloomy, at least in the short term. But not long ago, rhinoceros hornbills—the state emblem of Sarawak—were spotted in a nearby park. “I think the significance is huge,” Harrison says. “It suggests that if hunting is controlled, at least some species like the hornbills that can fly substantial distances could reestablish.” The hornbills might become an emblem of hope, a testament to the capacity of nature to heal.

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