Caterpillars crawl like none other: Unique means of animal locomotion has implications for robotics, human biomechanics

In an article published online July 22 in the journal Current Biology, the Tufts-led team reported that the gut of the crawling tobacco hawkmoth caterpillar (Manduca sexta) moves forward independently of and in advance of the surrounding body wall and legs, rather than moving along with them. Collaborating with Tufts were researchers from Virginia Tech and Argonne National Laboratory.

"Understanding this novel motion system may help efforts to design soft-bodied robots," said the article's senior author, Barry Trimmer, Tufts professor of biology and Henry Bromfield Pearson Professor of Natural Sciences in the School of Arts and Sciences. "It may also prompt re-examination of the potential role soft tissues play in biomechanical performance of humans and other animals."

Surprises Inside the Caterpillar

Anyone who has ever observed caterpillars knows that they crawl from back to front in waves. But advanced imaging reveals a surprising picture of what goes on inside.

The researchers used synchronized X-ray and visible light microscopy and videos to study the relative timing of movements of the crawling caterpillars' gut body wall and prolegs (unjointed leg-like structures on the mid-body that grip).

They found that the gut -- essentially a tube suspended at the rear and head of the caterpillar and decoupled from the body wall -- moved nearly a full step in advance of the surrounding structures. In contrast, gut movement was "in step" with motion of the head and rear.

Furthermore, points within the gut moved at different rates, suggesting that the gut was effectively shortening and lengthening during each crawl cycle.

"Although internal tissue movement caused by locomotion has been identified in many organisms, the caterpillars seemed to be propelling themselves by means of a two-body system -- the body wall container and the gut it contained. This may contribute to the extraordinary freedom of movement seen in these soft-bodied crawlers," said first author Michael Simon. Simon conducted the study as part of his doctoral research in Trimmer's laboratory, which focuses on how cell signaling contributes to the functions of the central nervous system and has extensively studied Manduca sexta.

In addition to Simon and Trimmer, authors on the paper included Tufts Research Assistant Professor William A. Woods; Tufts undergraduate Yevgeniy Serebrenik; Sharotka Simon, of Brandeis University; Tufts Graduate School of Arts and Sciences doctoral student Linnea van Griethuijsen; John Socha of Virginia Tech; and Wah-Keat Lee of Argonne National Laboratory.

More research is needed to determine if this phenomenon gives caterpillars an evolutionary advantage, in the same way that synchronizing breathing and tissue movements benefits running vertebrates, or arm swinging by walking humans increases stability and reduces metabolic costs.

Regardless, Simon says that this insight may offer valuable application to robotics. "The focus to date has been on robots' external design but we also have to look at how it's most advantageous to arrange the inside of the robot and any payload. Would motion be enhanced, for example, by packing more mass toward the rear, as these caterpillars seem to do?"

This work was funded by a National Science Foundation grant. Use of the Advanced Photon Source at Argonne National Laboratory was supported by the U. S. Department of Energy, Office of Science, Office of Basic Energy Sciences.