Visceral-Locomotory Pistoning in Crawling Caterpillars

Abstract

Animals with an open coelom do not fully constrain internal tissues, and changes in tissue or organ position during body movements cannot be readily discerned from outside of the body. This complicates modeling of soft-bodied locomotion, because it obscures potentially important changes in the center of mass as a result of internal tissue movements. We used phase-contrast synchrotron X-ray imaging and transmission light microscopy to directly visualize internal soft-tissue movements in freely crawling caterpillars. Here we report a novel visceral-locomotory piston in crawling Manduca sexta larvae, in which the gut slides forward in advance of surrounding tissues. The initiation of gut sliding is synchronous with the start of the terminal prolegs' swing phase, suggesting that the animal's center of mass advances forward during the midabdominal prolegs' stance phase and is therefore decoupled from visible translations of the body. Based on synchrotron X-ray data and transmission light microscopy results, we present evidence for a two-body mechanical system with a nonlinear elastic gut that changes size and translates between the anterior and posterior of the animal. The proposed two-body system--the container and the contained--is unlike any form of legged locomotion previously reported and represents a new feature in our emerging understanding of crawling.

A Model of Larval Biomechanics Reveals Exploitable Passive Properties for Efficient Locomotion

“…The Drosophila larva possesses a hydrostatic skeleton that runs the entire length of its body and is surrounded by a segmentally patterned cuticle and musculature. Kinematic evidence suggests that it moves using a two-phase visceral pistoning mechanism similar to that observed in Manduca sexta caterpillars [6,7] (Figure 1). During piston phase, the head, tail, and viscera of the organism move forward in a single step.…”

Common mechanics of mode switching in locomotion of limbless and legged animals

“…Caterpillars also use muscular movement involving peristalsis along the body axis. In some species of caterpillar, the body comprises a gut surrounded by a soft shell, which consists of the body wall (cuticle) and musculature; the former resembles a woven tube and the latter resembles a complicated, repeating series of primarily longitudinal and oblique muscles [2]. In some maggots, such as Neoempheria ferruginea, the occurrence of peristalsis is not clearly visible owing to transparency of the body wall.…”

Phase Contrast Imaging with Coded Apertures Using Laboratory-Based X-ray Sources

“…Recently there has been a lot of interest in the development of x-ray phase contrast imaging techniques and their application in various fields such as materials science and biology [1,2]. The main advantage of phase contrast imaging compared to conventional x-ray imaging is its increased sensitivity to small changes in the sample density and composition.…”

“…Stunning synchrotron phase contrast results have been demonstrated recently; for example, it became possible to perform in vivo studies of the processes associated with the breathing of insects [2]. It would be a great breakthrough for medical imaging and other modalities if phase contrast imaging methods could be transferred from the synchrotron environment into real-world applications.…”