The question Why did this animal evolve to do this?' can often be partly answered by asking What tries to eat this animal?' Evolutionary biologists have hypothesized that predator sensory systems in particular guide the evolution of how prey animals sense the world and how prey signals are sent. Aaron Rundus and colleagues at the University of California (Davis) recently tested this hypothesis by studying the kinds of signals California ground squirrels produce during snake attacks.

California ground squirrels are perfect bite-sized meals for many predators. Pacific rattlesnakes in particular appear to relish a squirrel snack. Rattlesnakes have evolved a highly sensitive heat-sensing organ,presumably to help them find glowing' mammalian prey. Ground squirrels, in turn, have evolved an impressive repertoire of defenses against the marauding reptiles. For example, when confronted with a snake, squirrels will puff up their tails and vigorously wave them in the snake's face (tail flagging')while simultaneously kicking up dust and dirt in an attempt to give the snake a good face full. Considering the unique heat-sensory abilities of rattlesnakes, Rundus and coworkers were curious to know whether tail flagging behavior had a thermal as well as a visual component.

In their first set of experiments, the researchers placed hapless ground squirrel volunteers in an enclosure with two different kinds of snake, one with heat-sensing ability (rattlesnake) and one that relies only on visual and olfactory cues while hunting (gopher snake). Understandably, in both situations, the squirrels showed vigorous tail flagging and other close-range snake defense behaviors. But thermal imaging revealed a more complex story. The squirrels significantly heated their tail regions when confronted with rattlesnakes, but not when going tail-to-face with gopher snakes.

In the rattlesnake's world, a hot tail swishing at high frequency might make a small mammal appear much larger and more threatening. To test the adaptive value of such a behavior, Rundus joined forces with a group of mechanical engineers and built a robotic squirrel. The Robo-Squirrel was a stuffed ground squirrel fully equipped with a motorized tail and controllable tail heater. Rattlesnakes are attracted to small baby rodents, so the research team tasked Robo-Squirrel with defending litters of rat pups from rattlesnake attack. When motorized tail flagging was present, rattlesnakes responded by moving less and orienting more towards Robo-Squirrel. These snake behaviors were enhanced when the robotic tail was fired up and began to emit a thermal signature. Furthermore, hot tail flagging by Robo-Squirrel drastically increased the amount of time rattlesnakes spent in two characteristic defensive postures (body coiled, body cocked to strike). These results suggest that hot tail flagging does indeed have adaptive value. The thermal display puts rattlesnakes on the defensive

Rundus and colleagues' simple (if you consider handling rattlesnakes simple) but elegant experiments demonstrate a novel form of animal communication. They show that an animal can use a biological fireworks display to ward off a specific species of heat-sensing predator. These results strongly suggest that the unique sensory abilities of a predator can indeed strongly mold the evolution of signaling in a prey animal. Just as important,this work highlights the limits of our own sensory abilities. As biologists,we have to be careful. If we don't try to see the world through the senses of the animals we work on, we might miss something beautiful and important.

Rundus, A. S., Owings, D. H., Joshi, S. S., Chinn, E. and Giannini, N. (
2007
). Ground squirrels use an infrared signal to deter rattlesnake predation.