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The similarity of crawling mechanisms in aquatic and terrestrial gastropods

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Abstract

Crawling gastropods are unique models for studying the functioning of smooth muscles and ciliated epithelia, since they cover the foot sole and are involved in locomotion, allowing for direct investigation. Two types of crawling are known: creeping by muscular waves in terrestrial gastropods such as Helix and сiliary gliding in aquatic gastropods such as Lymnaea. It was found that the smooth muscles that underlie the ciliated epithelium in Lymnaea are involved in gliding and contribute significantly to fast crawling. Thus, the locomotor apparatus is fundamentally the same in both snails and the difference between crawling reflects an adaptation to a habitat. The control of crawling speed is also the same. Tonic contraction, relaxation, and rhythmic contractions are involved in this control. During a locomotor episode, the sole length and crawling speed spontaneously change and directly correlate with each other via the contraction force of the muscle cells in the locomotory waves. Dopamine, unlike ergometrine, decreases the sole length and crawling speed. Serotonin stimulates, increases crawling and determines the number of muscle cells involved in the locomotory waves for each locomotor episode. This control (taking into account heterogeneity) apparently might exist in any other phasic smooth muscle, including vertebrates.

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Modified from Pavlova (2001)

Fig. 9

(modified from Trueman 1983; Denny 1981). The number of muscle cells involved in the wave is the same in b and c, but their contraction force is greater in b than in c (shown by the thickness and the length of muscle cells) as well as the work performed by the muscle wave (the area of the black rectangles W1 and W2). As a result, the crawling speed (V1 and V2 shown by the length of black arrows) is higher in the relaxed (b) than in the contracted (c) side of the sole (Pavlova 2001)

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Fig. 11

(modified from Trueman 1983; Denny 1981) before (e) and after (f) 5-HT injection. The contraction force of muscle cells in the wave (line thickness) is the same in e and f. The number of muscle cells in the wave is larger in f than in e and as a result, the work performed by the muscle wave (the area of the black rectangles W1 and W2) and the crawling speed (V1 and V2 shown by the length of the arrows) are greater in f than in e

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Acknowledgements

I am grateful to the Russian Foundation for Basic Research, which supported my study for years, including grant #13-04-01052. I thank all my colleagues who participated in this research and two anonymous reviewers who gave me useful recommendations and helped to improve the manuscript. The experiments complied with the ‘Rules of laboratory practice’ (RLP) in the Russian Federation no. 267 revised in 2003 from the Ministry of Health, with the current laws in Moscow State University, and they were also approved by the Ethics Committee of the A. N. Belozersky Institute.

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  1. A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow, 119899, Russia

    Galina A. Pavlova

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Pavlova, G.A. The similarity of crawling mechanisms in aquatic and terrestrial gastropods. J Comp Physiol A 205, 1–11 (2019). https://doi.org/10.1007/s00359-018-1294-9

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