Abstract
The design of a caterpillar's body forces it to walk slowly — but even though it cannot run away from danger, it can roll up quickly into a protective coil. Here, I show that the mother-of-pearl moth, Pleurotya ruralis, uses this reflex coiling as the basis for a method of high-speed escape. By anchoring the end of its body to the ground and recoiling against it, the larva converts itself into a backwardly rolling wheel. In doing this, it shows that the limitations of a soft, segmented body can be overcome, using the basic assemblage of segmental muscles, by temporarily sacrificing the need for stability.
Main
During forwards locomotion a wave of contraction followed by relaxation runs along the body from tail to head, producing the characteristic travelling ‘hump’1,2,3 on a caterpillar's back. As the wave passes, each segment is raised from the ground, is telescoped forwards into its neighbour in front, then is lowered back to the ground (Fig. 1a ). The legs attached to terminal segment 13 (claspers) and segments 6-9 are retracted, borne forwards with their segment, then put down again one ‘step’ ahead. Hence for the whole body to progress forwards one step, each segment needs to take its own step forwards. Each foot is airborne for only 35% of the cycle: although this maximizes stability it prevents the body from building up significant momentum. Caterpillar crawling is thus slow and uneconomical compared with terrestrial locomotion in animals with muscles harnessed to a rigid skeleton. Caterpillars walk at only 10% of the maximum speeds seen in adult running insects of the same weight4,5,6,7.
Like other moth larvae that seek protection inside rolled-up nettle leaves, the larva of Pleurotya ruralis lacks most of the normal caterpillar defences against birds and ichneumon wasps, such as cryptic coloration, irritant hairs or unpalatability8. But if an individual is isolated on a flat surface and provoked by mechanical shock, it displays a range of withdrawal responses of increasing speed and intensity, all based on locomotion in reverse.
Mild shock to the head or thorax elicits backwards walking, the exact kinematic inverse of walking forwards in that the peristaltic wave now begins at the head and moves tailwards. Stronger stimulation provokes a much faster wave, which arches up the whole body, wrenching all the legs free of the ground except the terminal claspers (Fig. 1b ). The latter now serve as an anchor to which the body can be jerked during its ‘airborne’ phase, until the intervention of the relaxation phase of the wave lowers the legs to the ground. As the relaxation wave reaches the claspers they detach, then reattach further back, thereby completing the step. Technically, this fast running retreat can be considered a ‘reverse gallop’ because the entire body (except the claspers) is airborne for a significant part of the locomotory cycle.
The third and most dramatic escape response begins like a reverse gallop but this time the relaxation wave fails to appear. The body continues to move under its own momentum, coils up into a wheel, and begins to roll backwards releasing the claspers as it goes (Figs 1c and 2 ). Depending on initial conditions, such as the flatness and texture of the surface, and any slight imbalances in the body during arch formation, the momentum is sufficient to produce up to five complete revolutions, and a withdrawal speed of 39±3.6 cm s-1 (n =31), nearly 40 times normal walking speed.
Recoil-and-roll uses the same set of segmental muscles as ordinary locomotion, but more quickly, dispensing with the need for serial contraction. The manoeuvre is derived from the basic coiling response of caterpillars under attack from their natural enemies. By harnessing the output of the flexural muscles involved in spiralling to a fixed point provided by the claspers, the caterpillar converts the coil into a rolling wheel. I have found no evidence for the involvement of an elastic spring in this mechanism, such as the pre-tensioning of the skin that allows maggots to leap up to 8 cm into the air9; on the contrary, recoil-and-roll makes maximum use of the power available from real-time muscle contraction.
References
Barth, R. Zool. Jb. 62, 507–566 (1937).
Hughes, G. M. & Mill, P. J. in The Physiology of Insects Vol. 3 (ed. Rockstein, M.) 335-379 (Academic, New York, 1974).
Brackenbury, J. H. Physiol. Entomol. 21, 7–14 (1996).
Casey, J. M. Science 252, 112–114 (1991).
Joos, B. Physiol. Zool. 65, 1148–1161 (1992).
Berrigan, D. & Lighton, J. R. B. J. Exp. Biol. 179, 245–259 (1993).
Berrigan, D. & Pepin, D. J. J. Insect Physiol. 41, 329–337 (1995).
Edmunds, M. Defence in Animals (Longman, London, 1974).
Maitland, D. P. Nature 355, 159–161 (1992).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Brackenbury, J. Caterpillar kinematics. Nature 390, 453 (1997). https://doi.org/10.1038/37253
Issue Date:
DOI: https://doi.org/10.1038/37253
This article is cited by
-
Multi-locomotion transition of tensegrity mobile robot under different terrains
Science China Technological Sciences (2023)
-
A study of ladder-like silk foothold for the locomotion of bagworms
Scientific Reports (2021)
-
A Four-legged Wall-climbing Robot with Spines and Miniature Setae Array Inspired by Longicorn and Gecko
Journal of Bionic Engineering (2021)
-
Rolling away: a novel context-dependent escape behaviour discovered in ants
Scientific Reports (2020)
-
Building Magnetoresponsive Composite Elastomers for Bionic Locomotion Applications
Journal of Bionic Engineering (2020)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.