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Caterpillars crawl like none other

Cell Press

Most of us have surely seen the slow and gravity-defying crawl of a caterpillar, with that wave of motion that passes over their elongated and flexible bodies. But it turns out that inside those crawlers, there's a completely different motion going on: their rather primitive guts slide forward before anything else moves at all.

The discovery, reported online on July 22 in Current Biology, a Cell Press publication, shows that caterpillars make their way through the world using a form of legged locomotion unlike any described before. In addition to expanding scientists' understanding of crawling, the researchers behind the discovery say that the new insights are finding their way into designs for soft-bodied robots of the future.

"From the outside, a wave progresses from the back of the caterpillar forward, and it looks like it all moves along with the wave," said Michael Simon of Tufts University. "But the gut moves around inside the body. It's a strange decoupled movement."

Simon, along with Tufts' Barry Trimmer and their colleagues, made the discovery completely by accident. Their interest is in neurosensory systems and the integration of sensory information to produce movement. To learn more about how caterpillars move, the researchers took some young hawkmoths to Argonne National Laboratory, where they could use sophisticated X-ray technology to see what was happening inside the caterpillars. They were expecting to find fluid sloshing around, Simon said. But instead, they saw what looked like the caterpillars' guts moving independently of the rest of their bodies. (Imagine for a moment your internal organs lurching upward on their own.)

The researchers characterized the crawling motion further using both X-ray and visible-light videos. Those videos showed that, at the start of each crawl, the gut in the insects' midbody segments moved in advance of the body wall and before the attached limbs, known as prolegs, swung. "The midgut typically advanced an entire step forward before the body wall caught up," the researchers report. In fact, the gut lurches forward and then falls back in what they describe as a pistoning motion.

There have been previous examples of internal tissue movements in mammals and birds, but those have always been the result of simple inertia. For example, Simon said, the livers of horses can slide back and forth as the animals gallop along.

"The unusual phenomenon of visceral-locomotory pistoning that we describe here is not generated by cyclic inertial forces from the locomotion itself, as in previous reports," the researchers write. In fact, most caterpillars move so slowly that they can stop and restart during any part of their crawl cycle without major changes in the movement of other parts of their bodies.

The caterpillar's anatomy is likely key. If you were to open a caterpillar up, you would see what is essentially an open bag lined with muscle, Simon explained. Their digestive system, a fairly simple tube running from the mouth to the anus, is suspended inside. And unlike what you'd find inside an earthworm, there are no walls separating one segment of their bodies from the next. That leaves the gut free to move in what the researchers refer to as "a two-body system--the container and the contained."

It's not yet clear whether this sliding gut movement has advantages for the caterpillars, the researchers say, but it certainly might. Because the young hawkmoths are all about eating and growing, it could be handy to free the gut from the disruptions of crawling.

The researchers think that what they've found in the hawkmoths will apply to other caterpillars and perhaps a few other creatures, including leeches. And they say that the findings are already contributing to efforts in their laboratory to design and develop robots made from soft materials, which might be better equipped than your average robot to squeeze into tight spaces or, like caterpillars, be "gravity agnostic." Simon says a free-floating "gut" might give such robots some very useful cargo room.

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The researchers include Michael A. Simon, Tufts University, Medford, MA; William A. Woods, Jr., Tufts University, Medford, MA; Yevgeniy V. Serebrenik, Tufts University, Medford, MA; Sharotka M. Simon, Tufts University, Medford, MA; Linnea I. van Griethuijsen, Tufts University, Medford, MA; John J. Socha, Virginia Tech, Blacksburg, VA; Wah-Keat Lee, Argonne National Laboratory, Argonne, IL; and Barry A. Trimmer, Tufts University, Medford, MA.

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