A Landscape of Fear

“Many biologists grew up viewing prey simply as animals waiting to be eaten, and if you didn’t get eaten, you were fine,” says Evan Preisser ’98, an assistant professor in the Department of Biological Sciences at the University of Rhode Island and a co-editor of a 32-page special feature on NCEs in the September 2008 issue of the journal Ecology. “But that’s akin to saying that if you were in a mall when a fight broke out and someone got shot, you were okay as long as you weren’t hit. In reality, even though this had no direct impact on you, it probably would have terrified you and, as a result, caused you to make all sorts of changes in your life. And if everyone present that day reacted the same way, even small changes in behavior manifested over a large population could have profound and unexpected effects. NCEs are, in essence, the wages of fear. The genius of Os’ work is that it gives us a much more nuanced view of reality.”

In the enclosures that had spiders, the grasshoppers changed both what they ate and when and where they ate it. P. mira is typically most active early in the day, but when the spiders and the grasshoppers were together in the cages, the potential prey shifted its peak activity and feeding period from morning to midday. The grasshoppers also tended to congregate in the relative safety of the upper reaches of the goldenrod. These tactics helped the insects avoid their predators, but at a cost—the increased risk of stress, sometimes fatal, from the heat. In addition, the spider-confronted grasshoppers ate considerably less of the bluegrass they preferred and turned more to the goldenrod and the wildflowers.

“When we subject them to the risk of chronic predation, they react just like we would.”
Dror Hawlena

By the end of the summer, the mini-meadows without spiders had different plant communities than those with resident arachnid predators. In the former, goldenrod, which can dominate its competition, held down the abundance and diversity of the grasses and wildflowers, such as clover, black-eyed Susan and wild strawberry. But where the nursery web spiders sat patiently and waited for a grasshopper meal, there was less goldenrod and a greater variety of the other plants.

This pattern held even in enclosures that contained spiders whose jaws had been glued shut by the researchers so that they could no longer hunt. The fear they continued to strike in their prey was enough to push the stressed grasshoppers into predator-avoidance mode—and the plant community into an altered state. (The operation, by the way, requires a gentle touch—the spider is held between two soft sponges while a dab of super glue is squirted between the jaws. This experimental strategy is possible only because nursery web spiders can go as long as two months between meals without starving to death.)

Schmitz looked at results he called “counterintuitive” and scratched his head. “If you’re not losing grasshoppers to predation, how can the spiders be affecting the plants?” he asked.

Then came an “Aha!” moment—the result, ironically enough, of a graduate school research project in behavioral ecology—and a bitter disappointment. A Canadian by birth, Schmitz started his research career in the late 1970s at the University of Guelph, where he studied the foraging behavior of deer and evaluated whether supplemental feeding programs were cost-effective. As a doctoral student at the University of Michigan, he examined deer foraging from an economics viewpoint, using a then-promising analysis tool called portfolio theory, to see whether deer were maximizing their returns by “investing” in a broad portfolio of food items that would minimize the risk of starvation.

“Unfortunately, by the time I finished my doctorate in 1989, this approach had been eclipsed by people interested in how avoiding the risk of predation shaped the behavior of animals,” says Schmitz. “I vowed to get out of behavioral ecology.”

But a landmark 1989 paper in Ecology by Thomas Schoener, a University of California at Davis community ecologist, changed his mind. Schoener, whom Schmitz calls his “academic grandfather,” and his colleague David Spiller looked at what happened to the animal and plant life on small islands in the Bahamas when the researchers manipulated the number of lizards present in experimental enclosures. The lizards preyed on web-building spiders, which, in turn, preyed on insects. Changing the number of lizards present not only had a direct impact on the spiders, but it also had an indirect effect on prey insects and the plants they consumed.

“The Schoener paper showed the value of looking at predators not just in terms of their interactions with prey, but also in terms of the myriad effects they could have in ecological communities of carnivores, herbivores and plants,” says Schmitz. “It offered me a way toward a more holistic perspective of entire systems.”

Aquatic biologists such as Bobbi Peckarsky, then at Cornell, had documented various aspects of these so-called trophic cascades in streams while investigating the interactions of trout, stoneflies and mayflies. But in the early 1990s, Peckarsky explained that her work and other aquatic studies like it weren’t commonly on the radar screens of terrestrial ecologists, who were still enmeshed in research about the direct effects of predation. “Os was the exception,” she says.

Schoener’s findings in the Bahamas and Schmitz’s conversations with Peckarsky and others provided “the impetus to get into food web work,” Schmitz says. Still, when he came to Yale in 1992, there was considerable doubt that indirect effects played a significant role in shaping terrestrial systems. “But no one had really looked,” he says.

The more Schmitz pondered his early results, the more he realized that the changes he observed in the grassland plants were not the direct result of prey being consumed and, thus, of there being fewer hungry herbivores in the meadow. Rather, he had documented an indirect effect: a predator causing a shift in prey behavior that, in turn, cascaded through the plants, as the grasshoppers switched to a less nutritious, but safer, diet.

This discovery and years of subsequent refinements of the key role played by what are now known as trait-mediated interactions—think, fear—almost didn’t happen. And here’s where serendipity came in. There’s another common spider in the meadow: Phidippus rimator. This jumping spider is an active predator, always on the hunt, and, unlike its sit-and-wait co-conspirator, never lingers in the same place for long.

When Schmitz examined this hunter’s impact on grasshoppers in the enclosures and in grasslands alike, he got different results. P. rimator knocked down prey numbers considerably, so there were fewer grazers to munch down the bluegrass. But because it was impossible for the grass-hoppers to determine where this predator was, the prey didn’t shift its behavior and diet toward the goldenrod and wildflowers.

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