Predators' fear of humans ripples through wildlife communities, emboldening rodents

Humans are top predators of many wildlife species, and our mere presence can create a "landscape of fear," according to researchers at the University of California, Santa Cruz. Fear of humans suppresses the movement and activity of pumas, bobcats, skunks, and opossums, which benefits small mammals. As their own predators respond to their fear of humans, deer mice and wood rats perceive less risk and in turn forage for food farther away and more intensively, they found.

The new study, "Fear of Humans as Apex Predators has Landscape-scale Impacts from Mountain Lions to Mice," appears in the July 17 online edition of the journal Ecology Letters.

"Humans are sufficiently scary to pumas and smaller predators that they suppressed their behavior and changed the way they used their habitats when they thought we were around," said lead author Justin Suraci, a postdoctoral researcher at UC Santa Cruz. "The most surprising part was seeing how those changes benefit rodents."

The findings are significant because as humans encroach on wild lands around the globe, ecologists are eager to understand the effects humans and development have on wildlife.

"We've spent 10 years learning how fear of humans drives mountain lion physiology, behavior, and ecology," said senior author Chris Wilmers, a professor of environmental studies at UC Santa Cruz and director of the Santa Cruz Puma Project. "This is the first large-scale experiment I'm aware of that documents how fear cascades through the food web from top predators to the smallest prey."

The research reveals that the presence of humans can have fairly profound effects, even without activities and infrastructure like hunting or housing or roads, said Wilmers, who studies human-wildlife interactions in California, Africa, and elsewhere.

"With human population growth and development, there is often a dual mandate to preserve wildlife and give people access to open spaces," he said. "This research starts to get at how we can realistically do both. We need to understand how animals react to our presence to make decisions and craft policies that protect their wellbeing."

Experiment design and results

Suraci and Wilmers designed a clever experiment that used recordings of human voices to assess the landscape-level effects of fear of humans. At two remote research sites in the Santa Cruz Mountains that are closed to public access, they placed 25 speakers in a grid pattern across a one-square-kilometer area. The speakers broadcast human voices, and recordings of tree frogs as a control.

Pumas, the researchers found, responded to the sound of human voices by significantly reducing their activity, keeping their distance, and slowing their movements. "When the frog recordings played, they would move right through the landscape," said Suraci. "But when they heard human voices, they went out of their way to avoid the grid."

Medium-sized predators changed their behavior in significant ways, too: Bobcats became much more nocturnal; skunks reduced their overall activity by 40 percent; and opossums reduced their foraging activity by a stunning 66 percent. "Bobcats pretty much gave up on daytime activity, shifting almost entirely to the night, when they presumably feel safer," said Suraci. "These predators aren't necessarily leaving the area, they're just less active, presumably because they're hiding more."

Over time, these behavioral changes could have dire consequences for pumas and the other predators if their food intake drops, said Suraci.

By contrast, deer mice increased their range by 45 percent, and the intensity of foraging by mice and wood rats increased by 17 percent. "They were apparently responding to the reduced activity of everybody else," Suraci added. "They're feeling braver, so they're moving around more and finding more food. They're not too averse to people, so they're taking advantage of the opportunity."

For wildlife, fear amounts to the perception of predation risk, explained Suraci. "Humans are incredibly lethal," he said. "We are major predators, and thus a source of fear, for a lot of these species. What's novel about this study is that we can see what that fear looks like in the environment at a relatively large scale."

Unlike studies that assess the impacts of development and subsequent habitat fragmentation, this research focused on the impacts of humans themselves.

"Just the fear of humans can affect how wildlife use the landscape and how they interact with each other," said Suraci. "It turns out, the mere perceived presence of humans triggers a disruption of natural predator-prey interactions -- and rodents really benefit."

Suraci is eager to investigate the relative impacts, or "cost/benefits," of living near humans for certain species. "Smaller carnivores don't want to interact with humans, but that may be outweighed by the benefits of feeding on trash -- and potentially being protected from pumas," he said. "We are working on some longer-term studies to explore that."

In addition to Suraci and Wilmers, the coauthors of the paper are Michael Clinchy and Liana Y. Zanette, both of the Department of Biology at Western University in London, Ontario.