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The Physical Properties of the Pedal Mucus of the Terrestrial Slug, Ariolimax Columbianus

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The Physical Properties of the Pedal Mucus of the Terrestrial Slug, Ariolimax Columbianus J. exp. Biol. (1980), 88, 375-393 375 With 15 figures ^Printed in Great Britain THE PHYSICAL PROPERTIES OF THE PEDAL MUCUS OF THE TERRESTRIAL SLUG, ARIOLIMAX COLUMBIANUS BY MARK W. DENNY* AND JOHN M. GOSLINE Department of Zoology, University of British Columbia, Vancouver, B.C., Canada, V6T 1W5 (Received 8 May 1980) SUMMARY The pedal mucus of gastropods functions in locomotion by coupling the movements of the foot to the substratum. The pedal mucus of the terrestrial slug, Ariolimax columbianus, is suited to this role by the following unusual physical properties. 1. At small deformations the mucus is a viscoelastic solid with a shear modulus of 100-300 Pa. 2. The mucus shows a sharp yield point at a strain of 5-6, the yield stress increasing with increasing strain rate. 3. At strains greater than 6 the mucus is a viscous liquid (rj = 30-50 poise). 4. The mucus recovers its solidity if allowed to ' heal' for a period of time, the amount of solidity recovered increasing with increasing time. INTRODUCTION The ventral surface of a gastropod's foot is separated from the sub-stratum by a thin layer of mucus. In many cases this mucus layer is left behind as the animal crawls, forming the slime trail that is characteristic of terrestrial snails and slugs. The importance of this pedal mucus in the locomotion and adhesion of gastropods has been known for a considerable time. Barr (1926) reports that slugs deprived of pedal mucus by cauterizing the suprapedal mucus gland can neither crawl nor adhere. Later authors (Lissman, 1945; Jones, 1973, 1975; Miller, 1974) speculate that pedal mucus serves as an adhesive in all gastropods, coupling the force of foot movements to the substratum. However, none of these authors have conducted tests to ascertain the physical properties of pedal mucus, and as a consequence its precise role has remained obscure. This study reports on the mechanical properties of the pedal mucus of the terrestrial slug, Ariolimax columbianus. These properties have been described briefly by Denny (1980a) and it will be shown here that A. columbianus pedal mucus is an unusual viscoelastic material, the properties of which are ideally suited to adhesive locomotion. Before describing the properties of this slug's slime it will be useful to briefly review the basic concepts, terminology, and testing procedures used in the study of viscoelastic materials. • Present address: Department of Zoology, University of Washington, Seattle, Washington, U.S.A., 98195. 376 M. W. DENNY AND J. M. GOSLINE TERMS AND TESTS If a force is placed on a material the material will deform, and if the material is elastic a given force will result in a unique deformation. This deformation will not change regardless of the time for which the force is applied, and if the force is removed the material will return to its original shape. The properties of elastic solids are quantified by normalizing force and deformation to the size of the sample being tested (see Fig. 1). The deforming force is divided by the area over which the force is applied to give the stress, <r. Similarly deformation is divided by sample thickness to give shear strain, y. The ratio of stress to strain is the material's stiffness, or shear modulus, G: G = cr/y. (1) The elasticity shown by soft materials is due to the presence of a crosslinked network of kinetically free, long, polymer chains. When the material is unstressed the chains assume a constantly changing, random configuration. When stressed, the material deforms; the chains pull on each other via the crosslinks, and are stretched to new, more ordered configurations. The change in entropy brought about by this change in configuration can be shown to account for the force required to deform the material. The statistical basis for this form of elasticity has been thoroughly studied and termed the theory of rubber elasticity (Flory, 1953; Treloar, 1970). The details will not be described here, the important point being that any elasticity found in a soft biological material (such as mucus) implies the presence of a crosslinked polymer network. The primary characteristic of fluids is that they flow. If a force is placed on a fluid the material will deform for as long as the force is applied; the greater the force, the faster the deformation. This property of fluids is quantified as viscosity, i], the ratio of stress to strain rate, y: V = No biological material is purely elastic or liquid, instead these real materials show a combination of these properties. To describe the properties of viscoelastic materials a number of standard techniques have been devised, the objective of which is to separately quantify the viscous and elastic contributions to the overall properties of the material. (1) Stress-strain tests. These tests are conducted essentially as shown in Figs. 1 A, B. A sample suitably held is subjected to an increasing deformation and the force measured at each strain. The deformation may be continued until the material fails, or at some point the deformation can be reversed and force measured as the material is returned to its original dimensions. Fig. 1E illustrates the property known as hysteresis, the loss of energy accompanying the cyclic loading of a sample. Hysteresis is a result of the viscous nature of a viscoelastic material. (2) Stress relaxation tests. If a material is quickly deformed to a given strain the stress required to maintain this strain can be measured as a function of time. If the material is a pure elastic solid by definition the force will not vary with time. If the material is a pure viscous liquid there is no force since the strain rate is zero. If the material is viscoelastic it shows a stress relaxation curve intermediate between the. Pedal mucus of the terrestrial slug, Ariolimax columbianus 377 Constant Force Strain,y Strain,y E deformation Fig. 1. Elastic solids and viscous liquids. (A) The dimensions of an undeformed sample. (B) The dimensions of a sample deformed in shear. Force is applied over area, A, the stress being force/area. Strain is the deformation, y, divided by sample thickness, x. (C) For an elastic solid stress is proportional to strain. (D) For a viscous liquid stress is proportional to strain rate, so that at a given strain rate there is a constant stress regardless of strain. (E) Energy is lost in the cyclic loading of a viscoelastic material. The area under a force-deformation curve is a measure of energy. The stippled area is the energy lost in the cycle shown. solid and liquid curves; the force gradually decays. An ideal viscoelastic material can be characterized by single values for elastic stiffness and viscosity, and in this case stress relaxes exponentially with time. The time needed to decay to i/e (37%) of the initial stress is known as the relaxation time and is a measure of the ratio of viscosity to elasticity. Real viscoelastic materials seldom show a single relaxation time, rather each infinitesimal volume of the material relaxes at a rate determined by the local viscosity and elasticity. There is thus a continuous distribution of relaxation processes occurring as the material as a whole relaxes. The relative number of elements relaxing at a certain rate is quantified as the relaxation spectrum, H(t). (3) Dynamic tests. As explained above, force for an elastic solid is proportional to the amount of deformation, while for a viscous liquid force is proportional to the rate of deformation. This fact is utilized in dynamic tests to separate the contribution of 378 M. W. DENNY AND J. M. GOSLINE elasticity and viscosity to the overall properties of the material. The material is deformed such that 7 = sin (at), (3) where co is the angular velocity (radians/second) and t is time (seconds). By reference to equation 1 the stress for a pure elastic material is; a- = Gy = G sin (cot) (4) and the stress is in phase with the strain. For a pure viscous liquid cr = TJ dy/dt, (from eqn 2) therefore cr = rj d(sin (o)t))/dt = r/ cos (cot) (5) so that stress for a viscous material leads strain by 900. A viscoelastic material shows a phase shift intermediate between a purely viscous or purely elastic material, i.e. somewhere between 90 and o°. Thus by measuring the phase shift, 8, between strain and stress a measure of the relative values of elasticity and viscosity can be found. At the same time the ratio of the stress amplitude divided by the strain amplitude yields a stiffness or modulus. This overall modulus (the complex modulus) is denoted G*. The elastic contribution to G*, cos 8 G* = G', is called the storage modulus, and is a measure of the energy stored in each cycle of deformation. Obviously G' = G* when 8=0° and G' = o when 8 = 900. The viscous contribution is sin 8 G* = G" or the loss modulus. The loss modulus is often used to calculate a dynamic viscosity, rj' = G"/o). The ratio of G" to G' is tan 8, a measure at low values that can be related to hysteresis. These three techniques form the basis for this study of the physical properties of A. columbianus pedal mucus. The knowledge gained from these tests can be used to: (1) predict the behaviour of a material in a given situation, and (2) provide some clue to the macromolecular structure of the material. MATERIALS AND METHODS Slugs were collected and housed as described by Denny (19806). Two types of testing machines were constructed to perform the tests described above, both machines designed to test thin layers of mucus in shear, under conditions as closely as possible approximating those under a crawling slug.
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