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Authors: Eric Dinerstein

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Hubbell may be correct in saying that trees so rare that only a single individual is found on average per fifty hectares could easily disappear. For example, tropical ecologists have discovered that the best germination sites for each species, such as open areas created by treefalls that are quickly shaded out, may be short-lived or unpredictable. Consequently, few of a tree's seeds may germinate or survive past the seedling stage. Yet trees that have evolved to live hundreds of years and produce 10,000 seeds per year have their own built-in protection for persistence. The production of viable offspring can afford to wait for the favorable but infrequent germination conditions that may depend on a fire, windstorm, or other event. After all, to be successful—to pass on its genes to the next generation—an individual need only replace itself once in a hundred years, and canopy trees live to be much older than that. The life history of a rare tropical canopy tree is a study in patience.

These hypotheses proposed to explain patterns of rarity in tropical trees are not mutually exclusive, and all are likely to be part of the answer. And, most interestingly, none is designed to explain how the large number of species was generated in the first place. That piece of the puzzle remains unsolved.

On a tranquil morning seven days after arriving in Madre de Dios, George, Sue, and I started back up the Tambopata. A heavy mist on the river kept the kingfishers grounded, but the sound of the outboard engine stirred awake slumbering capybaras on the floodplain islands as we approached. The world's largest rodents had found a safe haven from jaguars in the middle of the channels. There was not much green on the sand and stone beaches for their breakfast, but there were no big cats or anacondas, either.

After a night's rest, we continued our journey upriver before dawn, making our way to a blind created by some washed-up trees on a floodplain island. Across the channel an exposed clay cliff, about ten meters high, appeared before us like a vast canvas painted in a dull ocher wash, lifeless. “Just wait,” Sue whispered. “You won't believe this.”

With the first warming rays of the sun, flashes of blue, yellow, and gold flitted along the cliff face, followed by red and green with dashes of scarlet, blue, and chestnut. The
collpa
, or mineral lick, was alive with macaws and parrots, squawking and chewing on the mineral-rich earth. Not a handful of birds but hundreds of them represented five species of macaws—scarlet, red-and-green, blue-and-yellow, chestnut-fronted, and red-bellied—and at least nine species of parrots. We counted blue-headed, mealy, yellow-crowned, orange-cheeked, and white-bellied parrots, as well as dusky-headed, cobalt-winged, and white-eyed parakeets and, rarest of all, an albino blue-headed parrot. This must have been one of the densest concentrations of natural color anywhere. The macaws and parrots are believed to eat the earth to obtain sodium—an element in short supply in the food they normally ingest—and perhaps to help detoxify some of the chemically laced seeds they consume. There may also be social functions to this gathering. Whatever the causes, in this Kingdom of Rarities, the rare aggregation of multihued birds dazzled us—as did the swarms of brightly colored butterflies fluttering along the shoreline as we returned to the boat.

A cold front, known locally as a
friaje
, had moved upriver with us, and we spent the next two days in a chilly rain forest—who would imagine 10°C (50°F) in the Peruvian Amazon? The Madre de Dios region seemed caught in a collective shiver, and at night the temperature dropped precipitously. The effects of the friaje were most evident in the absence of local nocturnal wildlife seen or heard. We spent one night in a blind above a mineral lick usually frequented by salt-seeking tapirs. None appeared. Bats were scarce along the trails they typically used to commute between their roosts and their feeding areas. The silence was also conspicuous. Quiet
were the lead vocalists, the kinkajous—rain forest relatives of raccoons—the night monkeys, and the amphibians and insects that provide the background chorus.

That the cold weather disrupted the normal rhythms of the forest dwellers could explain what we saw late the next afternoon. We were heading back to camp when our sharp-eyed boatman pointed to a sandy stretch along the Tambopata floodplain. He slowed the boat and whispered, “
Mira!
Jaguar!”

Reclining on the beach was a large male jaguar. He was magnificent and quite unperturbed by the close approach of the boat. The driver turned the prow upstream, and we sat and watched the stationary cat. Ten minutes went by, then twenty. Perhaps the sandbank held the warmth of the sun's rays in the approaching dusk, and after a frigid week in the forest the jaguar was content to rest and warm his bones. We were so enraptured by our sighting that we ignored a smaller boat idling nearby until we noticed the three men in the craft eyeing the same splendid cat. Tucked below the gunwale was a barely concealed rifle. To foil the hunters, we waited until it grew too dark for them to see the outline of the jaguar. With no chance for a kill, the men headed back downriver. We disembarked and walked toward the jaguar, urging it back into the forest for its own protection. In their years in Peru, George and Sue had never seen such a calm jaguar, much less have to save one from other humans.

That evening, the unforgettable encounter with both predator and poacher was at the center of our conversations. “George, if the poachers had arrived before we did, there would have been one less jaguar hunting along the floodplain of the Tambopata. But take it to the extreme. What if protection broke down completely and hunters shot every last jaguar in these parts? How would this ecosystem be different?”

George didn't hesitate. “You remember John Terborgh's studies in Venezuela at Lago Guri, don't you?” George was referring to one of conservation biology's leading field men, a hero to us. Terborgh's
innovative natural experiment in Venezuela involved censusing the inhabitants of islands created by dam impoundments in once continuous forest. Some of the human-made islands were too small to support even a single jaguar or other felid. Terborgh showed that when such top predators are lost in a system, the forest changes rapidly because there is a swift increase in the numbers of sloths, monkeys, deer, and peccaries that eat plant matter and all the midsized vertebrates that eat insects. The forest's low vegetation becomes less dense because populations of species such as leaf-cutting ants explode; while the howler monkeys defoliate the tree canopy, the ants clear out the understory. The absence of large carnivores creates a different kind of kingdom, minus the usual ecological checks and balances, and allows, at least for a short time, explosive growth of certain herbivores—mammalian and insect.

The impact that rare top predators can have on ecosystems was made even clearer in 2011. In a review paper in the journal
Science
, James Estes, John Terborgh, and their colleagues introduced a new phrase into the ecological lexicon: the “trophic downgrading of planet Earth.” On land, in streams and lakes, and in the sea, the removal of apex predators—jaguars, pumas, salmon, sea otters, sharks—has had a profound and cascading effect, termed “trophic cascades,” on the species layered under them in the food pyramid. The Terborgh study in Lago Guri mentioned earlier was but one example of a trophic cascade that had many parallels in other biological realms. The loss of sea otters, for example, had a profound effect on the distribution of kelp forests as the urchins that grazed the kelp were no longer kept in check by the otters. All of the species that depended on the dense kelp forests for food and habitat were affected. In freshwater systems, the drastic reduction of native salmon runs has reduced the amount of enrichment that occurs upstream as salmon spawn and die and their decomposition releases vital nutrients into the system. Other fish also become more prevalent in the absence of this predator. On land, removing the top predators means that the effects trickle down in the ecosystem,
reducing the productivity of the soils, the diversity of plants, and the amount of carbon sequestered in forests.

Terborgh's long-term study, begun in 1990, of what had become virtual island ecosystems ended around 2005 with a surprising outcome. It supported one of the signature theories about how the natural world works: that the tropical world is green only because leaf-eating creatures, from howler monkeys to leaf-cutter ants to insect larvae, are kept in check by their predators. At the same time, it unexpectedly undermined an opposing argument, that the nasty chemicals in the leaves were enough to keep herbivores at bay. This top-down effect large predators exert on the ecosystem stands opposite the bottom-up effects we saw in the operation of the invertebrate leaf and seed eaters in regulating the distribution of tropical trees. Both may be at work at the same time.

The role of peccaries is also important in shaping the Amazon rain forest in this region. Peccaries consume fruit and seeds from more than 400 plant species, far more than any other fruit eaters in the forest. They likely disperse the seeds of about 250 of the ingested species but act as influential seed predators for the other 150 species. They also trample many seedlings and suppress their recruitment. But for peccaries to have such a landscaping effect on the forest they need to be abundant, not nearly hunted out and rare. On the other hand, should jaguars and pumas disappear, the interactions between peccaries and plants would increase with their populations and change the composition of the forest. Harald Beck, a peccary biologist and Terborgh protégé, found that in areas where peccaries no longer roamed freely because they were hunted out, there was a dramatic increase in seedling dispersal of a common palm genus,
Iriartea
, whose seeds peccaries destroy in consumption. Peruvian forests without peccaries and jaguars look different from forests where they have been present, in part because palms are less common in the understory when those species are present. Peccaries, along with rhinos elsewhere, certain other large mammals, and some birds, are able to serve as ecosystem engineers. As
such they play vital ecological roles, often disproportionate to their numbers or biomass, in shaping the structure and species makeup of the rain forests. These are keystone species: their demise often triggers a collapse or a dramatic change in that system, much as the keystone in an arch is an essential piece in the design of that structure. The loss of a keystone species often triggers a trophic cascade.

Of course, one doesn't have to purchase a ticket to Puerto Maldonado, or any tropical wildland, to see the effects of such a phenomenon. A walk through a deciduous forest in the eastern United States illustrates the ecological damage of an ongoing trophic cascade. The eradication of pumas and wolves from these forests, along with their fragmentation, has led to a proliferation of white-tailed deer. Absent their predators, deer have become a nuisance to motorists and gardeners and a health threat, serving as hosts for the ticks that spread Lyme disease. The change has not been good for native birds such as wood warblers, either. The understory vegetation in many eastern forests has been greatly reduced or even eradicated by the hungry hoofed mammals. As a result, the hooded warbler, worm-eating warbler, Kentucky warbler, and Canada warbler, among other species that nest on or near the ground, have declined because overbrowsing by deer exposes their nests and nestlings to predators.

In the rain forest, monkeys also serve as a great example of keystone species in the canopy. I mentioned to Sue one day as we were scanning the canopy for primates, “Your saki monkeys are probably safe from hunters because of their cryptic behavior . . . But what about spider monkeys? Don't hunters consider them a delicacy? Do we know what happens when a forest loses its fruit-eating monkeys?”

“Spider monkeys are often the first to be hunted out in most rain forests,” Sue responded. “It seems animals that eat mostly fruit—spider monkeys, macaws, parrots—all have tasty meat the hunters go for.” Then Sue mentioned the work of a World Wildlife Fund postdoctoral student, Gabriela Nuñez-Iturri, who compared seedling
presence and abundance in areas where spider monkeys and other fruit eaters are still common and protected with that in areas where these species have disappeared. At sites where primates had been hunted for thirty to forty years, seedlings and small juvenile trees whose seeds are dispersed by the larger primates were reduced by nearly 50 percent, whereas the seedlings of wind- and gravitydispersed plants became 284 percent more common. Her study showed that the composition of seedling and small juvenile tree species that ultimately regenerate future forests differ markedly in hunted forests as compared with protected forests where primates and large fruit-eating birds still thrive.

The loss of the big, rare tropical trees from logging would also have a dramatic ecological effect. By combining Greg Asner's laserscanning data on the carbon density of the rain forest with the information Sue, George, and Gabriela had gathered, we have recently learned even more about how the fates of jaguars, monkeys, macaws, and peccaries and the future of tropical forests are closely linked. The tree species that hold the most carbon in the forest are the ones with the densest wood and with seeds that are dispersed by birds and mammals, and they are typically rare per hectare. If those birds and mammals disappear as a result of hunting, the rare trees over time are likely to be replaced by an aggregation of trees that have much lower carbon densities and much lower diversity. If soaking up carbon dioxide is a global benefit conferred by tropical rain forests, then monkeys and large fruit-eating birds, by the seeds they disperse, help to create the most carbon-dense forests. We can thus see how the loss of primates and birds from a rain forest not only removes a keystone species but also contributes to a trophic cascade, a process that typically leads to a more impoverished, less stable environment.

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