A tobacco hornworm moving along a wooden stick. Photo credit: Barry Trimmer.

A tobacco hornworm moving along a wooden stick. Photo credit: Barry Trimmer.

Unrestrained by a skeleton, tobacco hornworms are remarkably agile pests, rippling their bodies to scale tomato and tobacco plants, ready to gorge in preparation for their miraculous transformation into adult moths. The adaptable insects are capable of contorting themselves to remain in contact with almost any surface, ranging from stable ground to fluttering leaves, while manoeuvring between dining opportunities. But Barry Trimmer from Tufts University, USA, explains that the moth larvae's squidgy bodies pose a unique set of challenges as they shuffle along. ‘Soft, deformable animals face very different biomechanical challenges compared with articulated animals’, he says. For example, animals equipped with skeletons often change stride when they encounter a new surface or switch to climbing a hill, which made Trimmer wonder whether the versatile caterpillars also adapt their movements when encountering a new situation. Together with Cinzia Metallo and Ritwika Mukherjee, Trimmer began investigating how the distinctive caterpillars crawled on soft and hard, vertical and horizontal surfaces, to find out whether they adjust their stride.

After building a caterpillar-sized treadmill and constructing a super-springy Dragon Skin® silicone drive belt for the insects to saunter along, the trio set three hornworms strolling horizontally before flipping the treadmill upright and setting the caterpillars crawling upward and downward as they filmed the insects’ footwork. They also tested the insects’ manoeuvres as they scaled and strolled along a more rigid rubber walkway, to find out whether the creepy-crawlies adjusted their stride.

Then, the scientists focused on the four prolegs – which bear the rear end of the 70 mm long insects – as the caterpillars crawled horizontally on the most rigid treadmill belt. The majority of the time, the plump caterpillars concertinaed the body forward at the start of a stride, lifting the rear-most proleg (the sixth) first, before the fifth, fourth and third rippled up. Then, once all four prolimbs were off the treadmill, the caterpillar lowered its sixth proleg back down as it extended its body, swinging each proleg forward and placing it in turn on the treadmill belt. However, on 20% of occasions, the smoothly rippling legs fell slightly out of sync, with the sixth proleg touching down on the treadmill before the third proleg was raised. ‘This change in rhythm is reminiscent of the way other animals change gait at different speeds or to accommodate a new terrain’, says Trimmer. The team also scrutinised the caterpillars ascending the treadmill vertically, noticing that the caterpillars resorted to this alternative footfall pattern more often, replacing the sixth proleg before raising the third 51% of the time, while the descending caterpillars preferred the alternative gait 65% of the time. And, when they provided the caterpillars with the springier Dragon Skin® treadmill belt, the insects relied much more on the stability of replacing the sixth proleg before the third lifted up, resorting to it 46% of the time on the flat, 73% when climbing and almost 80% when descending.

‘Our results show that caterpillars change their stepping patterns when they climb in different directions or when they are on different surfaces’, says Trimmer, adding that the caterpillars seemed to prefer stride patterns with more prolegs in contact with the treadmill for stability when the going was soft and when tackling an ascent or descent. The results also suggest that caterpillars are able to sense differences in the materials over which they are moving and adjust their stride accordingly. ‘These findings make us wonder how the stepping patterns are controlled by the nervous system and how caterpillars can tell that they are walking on different surfaces’, says Trimmer, who is curious to understand how the larvae feel these differences.

References

Metallo
,
C.
,
Mukherjee
,
R.
and
Trimmer
,
B. A.
(
2020
).
Stepping pattern changes in the caterpillar Manduca sexta: the effects of orientation and substrate
.
J. Exp. Biol.
223
,
jeb220319
.