Wild birds: A trip to the market reveals species imperiled

Wild Birds

“Wild birds are being vacuumed out of the forests, gardens and fields of Indonesia, and we have to quickly figure out which species are in danger of extinction.” –David Wilcove, professor of ecology and evolutionary biology and public affairs in the Woodrow Wilson School

THE SIGHT OF A SOUTHEAST ASIAN BIRD market rivals the din of one for being overwhelming. Thousands of wild-caught birds are packed into cages that hang from eaves and fill market stalls to the ceiling, lining the paths trod by prospective buyers like a living wall. Taken from fields and forests, these birds are prized for their song, their colors, their spiritual significance or their long-time association with status and wealth. For the people who come to these markets, the birds — young and old, endangered and common — have meaning and value.

But to scientists, conservationists and governments, the wild-pet trade is a destructive yet unmonitored and elusive force on wildlife populations.

Princeton University researchers went deep into the wild-bird markets and trapping operations on the Indonesian island of Sumatra to document the draining of species by the pet trade. They found there a new and interesting weapon in the struggle to gauge — and halt — the devastation of the wildlife trade on animal populations: the very markets where the animals are bought and sold.

Species that are disappearing as a result of the pet trade can be identified by changes in their market prices and trade volumes, a study led by the Princeton researchers found. The researchers studied open-air pet markets on Sumatra from 1987 to 2013 and found that bird species that increased in price but decreased in availability exhibited plummeting populations in the wild.

The researchers concluded in the journal Biological Conservation in July 2015 that a prolonged rise in price coupled with a slide in availability could indicate that a species is being wiped out by its popularity in the pet trade. Through regular pet-market monitoring, conservationists and governments could use this information as an early indicator that a particular species is in trouble, the researchers reported.

Lead author Bert Harris, who was a postdoctoral fellow in the Program in Science, Technology and Environmental Policy in Princeton’s Woodrow Wilson School of Public and International Affairs when the work was conducted, said that market monitoring can be done far more quickly and cheaply than field-based monitoring of wild populations.


Birds such as the Oriental white-eye (top photo ) are packed into tight cages where they are at risk of disease. Many Asian and African countries host a startling number of species yet have lax-to-nonexistent monitoring and conservation programs. The Princeton researchers’ market-monitoring method can be done far more quickly and cheaply than field-based monitoring of wild populations. PHOTO COURTESY OF DAVID WILCOVE

One important function of the study is to highlight the pet trade as an emerging threat facing many birds and other wildlife, one that can act independently from other drivers of extinction such as habitat loss, said senior author David Wilcove, a professor of ecology and evolutionary biology and public affairs in the Wilson School.

He and Harris worked with co-authors Jonathan Green, who was a Princeton postdoctoral researcher in the Wilson School and is now at the University of Cambridge; Xingli Giam, who earned his Ph.D. at Princeton in 2014 and is now at the University of Washington; and researchers from the Wildlife Conservation Society and the Indonesian Institute of Sciences.

“Wild birds are being vacuumed out of the forests, gardens and fields of Indonesia and we have to quickly figure out which species are in danger of extinction,” Wilcove said. “We’ve got to change how we tackle this problem.”

Carter Roberts, president and CEO of the World Wildlife Fund, said that the researchers’ use of wildlife-trade market data to identify endangered species is a “potentially breakthrough idea.”

“What I think makes this paper so exciting is that it suggests a two-pronged approach to addressing the threat to biodiversity posed by the wildlife trade: using market data to identify the species that are likely being severely overexploited, and then targeted research and conservation efforts at those species,” Roberts said.

The researchers found that 14 birds popular in Sumatran pet markets were identified by local experts as declining or severely declining — yet, only two are officially recognized as imperiled. In addition, only two species are restricted to old growth forests, meaning that deforestation alone could not explain the declines. The pet trade was clearly a culprit, too. Furthermore, the researchers found that six species that are not popular as pets exhibited population increases. The researchers confirmed their method by studying the cases of two birds that are critically endangered by the pet trade — the yellow-crested cockatoo and the Bali myna.

Existing studies have explored wildlife markets, but only documented a species’ market volume, or availability, Harris said. The Princeton-led study, which was supported by the High Meadows Foundation, is the first to consider price and market volume. Market availability alone can fluctuate for reasons unrelated to a species’ wild population, such as a decrease in popularity, he said.

During the course of the research, Harris visited bird markets to gather price and availability data. They are chaotic places where Westerners asking about prices are viewed with suspicion.

“The markets are the dirty part of conservation,” Harris said. “They’re noisy and smelly. And after someone who looks like me asks about prices two or three weeks in a row, sellers just stop responding.”

Wilcove was inspired to conduct the current research after a trip to Sumatra when he noticed a prevalence of wild-caught pet birds. Research has found that 22 percent of Indonesian households own birds.

One bird the researchers identified as declining in the wild, the white-rumped shama, which is prized for its song, can be raised in captivity. Yet people seem to prefer the wild individuals, Wilcove said. He and Harris want to explore how governments and conservation groups can convince people to keep captive-raised birds.

“It’s time for some new approaches,” Wilcove said.

–By Morgan Kelly

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Striking resemblance: A physical law may govern very different biological activities


FLOCKS OF BIRDS FLY ACROSS THE SKY in shifting configurations. In the retina of an eye, millions of neurons ignite in ever-changing combinations, translating light into meaningful images. Yet both of these seemingly random behaviors have an underlying order that can be described by mathematics.

Like these cells and birds, when atoms and molecules come together they can display coordinated behaviors that are more than the sum of their parts. At a critical point, such as the boundary between liquid and gas, local interactions between molecules propagate through an entire material, changing its essential properties.

Princeton biophysicist William Bialek thinks criticality may also underlie collective behaviors in living organisms, and he’s using real-world data to test this hypothesis. Recently, Bialek and his colleagues have analyzed the flocking behaviors of birds, the genetic networks of fruit fly embryos and the activation patterns of salamander neurons.

“In physics, we use the same mathematical language to describe many seemingly different behaviors,” said Bialek, the John Archibald Wheeler/Battelle Professor in Physics and the Lewis-Sigler Institute for Integrative Genomics. “So we understand that the emergence of collective behavior from all the individual interactions has a kind of universality.”

To explore the possibility that this universality might extend to living systems, Bialek made use of a large dataset on the changing positions and velocities of thousands of individual birds in a flock of starlings. A group of Italian physicists used multiple cameras to record the birds and calculate their exact locations over time in three dimensions — “a technical triumph,” according to Bialek.

The researchers, including former Princeton postdoctoral fellows Thierry Mora and Aleksandra Walczak, analyzed the deviations of each bird from the flock’s average speed and direction of movement. They found not only that these variations were correlated between nearby birds, but also that the fluctuations from the average propagated through the group over long distances. This pattern of rapid, remote signal transmission echoes the changes that occur among molecules during a phase change from solid to liquid or liquid to gas. At a critical point, this could allow information to spread swiftly through the group, enabling the whole flock to nimbly change direction.

“The model you build just by keeping track of what each bird does relative to its neighbors predicts what happens throughout the entire flock,” Bialek said. “And it does so with an accuracy that is beyond what we had any reason to expect. It’s really a very precise prediction.”

Other biological examples of criticality play out on a microscopic scale. Bialek has an ongoing collaboration with Princeton’s Squibb Professor in Molecular Biology Eric Wieschaus, a Howard Hughes Medical Institute researcher and Nobel Prize winner, who has uncovered many of the genes involved in the embryonic development of the fruit fly — a model biological system.

Bialek has found signatures of criticality in gene activation patterns during the first few hours of fly embryo development. The synchronized actions of “gap genes” establish the fly’s 14-segment body plan. Mutations in these genes lead to gaps between segments, whose effects are reflected in the names of the genes: two examples are “hunchback” and “giant.”

Recently, Thomas Gregor, an assistant professor of physics and also a member of the Lewis-Sigler Institute, has developed experimental tools to precisely measure the activity of many gap genes at once, all along the halfmillimeter length of the fly embryo. These measurements allowed Bialek and physics graduate student Dmitry Krotov to test whether the patterns of gene activity across the embryo fit a model of criticality. Indeed, using data from 24 embryos, they found that fluctuations from the average level of gene activity at each point along the embryo were correlated between certain pairs of gap genes, which regulate one another’s activity like on/off switches. They mapped the locations of these switch points, which appear to act like signals that spread over long distances, just as changes in velocity are correlated in a flock of birds.

Bialek has also looked for signatures of criticality among the activation patterns in a patch of 160 nerve cells from a salamander retina, a model system for studying this light-sensing layer of the eye. In collaboration with Michael Berry, an associate professor of molecular biology and the Princeton Neuroscience Institute, Bialek and his colleagues showed how the coordinated activity of the neurons could be tuned to a critical state.

Bialek thinks critical systems may be common features of life that have repeatedly evolved in different organisms and at different levels — both molecular and behavioral. This could explain why, though systems of cells or groups of organisms could be organized in any number of possible ways, networks with similar properties continue to emerge.

“Is there anything special about the way nature has organized things in living systems?” Bialek wondered. He said much more work is necessary to claim criticality as a general biological principle. “But I do think we’re seeing in the data, somehow, signs of that specialness — things that it seems you can only get if the system has been set up in particular ways and not in others,” he said. “That I find very appealing.”

This work was supported in part by the National Science Foundation, the National Institutes of Health, the Howard Hughes Medical Institute, the W.M. Keck Foundation and the Swartz Foundation.

–By Molly Sharlach