The role of mucus in the locomotion and adhesion of the pulmonate slug, Ariolimax Columbianus

Gastropod snails move using a single appendage - the foot. For many gastropods the power of locomotion is provided by muscular waves moving along the ventral surface of the foot, the force of these waves being coupled to the substratum by a thin layer of mucus. This mucus acts as a glue which causes the animal to adhere to the surface upon which it crawls, but nonetheless allows forward movement of the animal. In fulfilling this function the mucus must show some unusual properties. This study examines the chemical and physical properties of the pedal mucus of the pulmonate slug Ariolimax columbianus, and relates these properties to the role of mucus in locomotion. The pedal mucus of A. columbianus is a gel consisting of 96-97% water restrained by a network formed of a high molecular weight glycoprotein. The glycoprotein is a polyelectrolyte; the charged nature of the molecule causing it to swell in solutions of low ionic strengths. This swelling accounts for the glycoprotein's ability to influence a large volume of water. The gel network is stabilized both by disulfide bonds between protein moieties, and by "weak bonds" (hydrophobic interactions and/or hydrogen bonds) between glycoprotein molecules. The physical properties of the pedal mucus were measured in shear. At shear ratios of less than 5, and over short time periods, the gel shows the properties of a viscoelastic solid. G' is 100 N/m2₂ and tan d is 0.008; both are virtually constant from 0.1 - 100 Hz. Over long periods of time the gel stress relaxes without reaching equilibrium, indicating that the weak bonds of the gel network allow the network to flow under stress. At a shear ratio of about 5 the gel network yields as weak bonds are broken, and with further deformation the mucus acts as a viscous fluid with a viscosity of about 50 poise. If this fluid is allowed to stand unstressed, the gel network will "heal" as the weak bonds reform. This healing process begins in much less than a second and, as a result, the mucus again acts as a solid. This "yield-heal" cycle can be repeated numerous times. These physical properties are ideally suited to gastropod locomotion. Under the moving portions of the foot (the muscular waves and the rim) the mucus is present in the form of a viscous liquid, lubricating forward motion. Under the stationary parts of the foot (the interwaves) the mucus has "healed" and, as a solid, serves as an effective adhesive. The mucus thus acts as a material ratchet allowing for effective adhesive locomotion. The precise movements of the foot of columbianus were measured using a video tape recorder. The thickness of the mucus layer was measured by quickly freezing, and subsequently sectioning, crawling slugs. These data, along with the measured physical properties of pedal mucus, allow for the construction of a model predicting the forces operating under a crawling slug. This model has been tested by actually measuring these forces, and has proven accurate. The increased oxygen consumption associated with locomotion in A. columbianus was measured as a function of crawling speed. From these data the cost and efficiency of adhesive locomotion have been calculated. Movement of &. columbianus is about ten times as costly as for a mouse of the same weight. This high cost is largely due to the cost of producing the pedal mucus. While the cost of adhesive locomotion is high, the efficiency of locomotion is roughly equal to that of a running man. It is very likely that the measurements and predictions made in this study will apply to all terrestrial pulmonates; and it is possible that they will apply to other gastropods as well.Science, Faculty ofZoology, Department ofGraduat