5.4 Protection
The use of mucus to isolate an animal from its environment, or to actively counter some facet of environment is common in marine Mollusca and it is perhaps here that mucus is most diverse in function. Mucus is produced from most molluscan epithelia (Simkiss and Wilbur, 1977), acts as a barrier to diffusion (Grimm-Jørgensen et al., 1986) and may function in selective ion transport (Ahn et al., 1988).
Gastropod epithelial mucus is often a first line of defence and has been shown to reduce exposure to physical stress and predation. Wilson (1929), Bingham (1972), Morris et al. (1980), Denny (1984), McMahon and Britton (1985), Britton (1995) and Davies and Hawkins (pers obs.) have noted the habit of littorinids and amphissids of attaching themselves to vertical rock using a strand of pedal mucus as a glue between substratum and shell. The animal’s head is then retracted behind the operculum. This behaviour is thought to render the animal less susceptible to desiccation and overheating. By secreting a veil of mucus (which then dries to form a wall) between shell and substratum, the limpets Acmaea (Tectura) digitalis, A. (Macclintockia) scabra and A. persona can reduce desiccation stress (Wolcott, 1973). A similar phenomenon occurs in terrestrial snails which secrete a CaCO3/ mucus matrix across the shell aperture which dries to form a water-tight seal (e.g. Helix aspersa, Otala lactea, Sphincterochila boisseri,Machin, 1967; Schmidt-Nielsen et al., 1971). Mucus has also been implicated in protecting antarctic limpets from extreme cold (Hargens and Shabica, 1973). The role of mucus in fish as a barrier to pollution has been extensively studied (Shephard, 1994), but in molluscs this has not been directly assessed. However, excess mucus production by bivalves after exposure to heavy metals (Lakshmanan and Nambisan, 1985; Moraes and Silva, 1995; Sunila, 1987; Hietanen et al., 1988; Sze and Lee, 1995) and hydrocarbons (Axiak and George, 1987) has been reported; and excess pedal (Mills et al., 1990) and intestinal (Triebskorn, 1989; Triebskorn and Ebert, 1989) mucus production by slugs in response to metaldehyde (a molluscicide) has been observed. Davies (1992) described a reduction in pedal mucus production in limpets, Patella vulgata, exposed to single heavy metals, although this reduction was probably owing to an accompanying lack of activity. Mucus can function in predator avoidance by rendering the gastropod distasteful and/or toxic (e.g. the dorsal secretions of Doriopsilla albopunctata,Reel and Fuhrman, 1981 and Phyllidia varricosa,Johannes, 1963; the hypobranchial mucus of Calliostoma canaliculatum (pers. comm., N. Smaby); the secretions of the mantle edge in Cellana spp., Branch and Branch, 1980); by anaesthetizing the predator (Trimusculus reticulatus,Rice, 1985); by fouling the predator’s feeding apparatus (e.g. Ariolimax columbianus,Richter, 1980); or by making the animal too slippery to handle (e.g. Calliostoma species, Sellers, 1977; Harrold, 1982). Handling of molluscs can also induce copious mucus secretion (e.g. Buccinum undatum, Strombus gigas pers. obs.), as can tissue disruption upon dissection (e.g. Milax sowerbii,Barr, 1926; Archidoris pseudoargus,McCance and Masters, 1937). Interestingly, some nudibranchs are able to sequester poisons from their food which subsequently emerge in their mucus, providing a defence for these molluscs which cannot retreat into a shell. Indeed the evolution of loss of shell in this group may well have coincided with the ability to use mucus in a defensive capacity. Poisons or deterrents will probably all emerge with mucus, but few studies have specifically recognized this. Examples include: Avila et al. (1991) who observed that Hypselodoris webbi secretes the allomone longifolin (an ichthyodeter-rent) in its dorsal mucus, the allomone originating in the sponge Dysidea fragilis;Paul et al. (1990) who observed that Nembrotha spp. secrete tamb-jamines (ichthyodeterrents from the ascidian Atapozoa sp.) in their mucus; Gustafson and Andersen (1985) who discovered terpenoids from sponges, bryozoans and coelenterates in the mucus of Archidoris montereyensis and Anisodoris nobilis.
The African land snail Achatina fulica produces an agglutinin (lectin) in its mucus (Iguchi et al., 1985) which is a 70 000 MW glycoprotein (Mitra et al., 1988). Lectin activity has also been reported for the mucus of the terrestrial gastropods Arion empiricorium (Habets et al., 1979), Helix aspersa (Fountain and Campbell, 1984; Fountain, 1985) and Archachatina marginata (Okotore and Nwakanma, 1986). Astley and Ratcliffe (1989) examined the mucus of some species of marine mollusc but could find no lectins, although they were present in the epithelial mucus of Loligo vulgaris (Marthy, 1974). Whilst these discoveries present numerous potential roles for mucus (slug mucus is apparently used in some human therapy, Habets et al., 1979), it may be that the lectin has no function other than structural within the mucus matrix (Fountain, 1982). McDade and Tripp (1967) recorded the presence of lysozyme in oyster mucus and hypothesized that this formed an antimicrobial defence, although lysozyme may merely prolong the functional life of the mucus by slowing down bacterial breakdown. Kubota et al. (1985) purified a glycoprotein (“achatin”, 140 000 MW) from the pedal mucus of Achatina fulica which showed no lysozyme activity but did kill both gram-positive and gram-negative bacteria by acting on cytoplasmic membranes (Otsuka-Fuchino et al., 1992). The use of mucus as a carrier for these compounds provides an unstirred layer on the surface of the animal in which the compounds can be held and prevents them from dispersing in an aquatic environment (Denny, 1989). Bakus et al. (1986) reviewed the chemical ecology of marine organisms and whilst they rarely mentioned mucus it is likely that mucus is employed as a carrier of secretable chemicals in most of the taxa they describe.
The functioning of limpet pedal mucus in limpet tenacity (to prevent dislodgement by, for example, predation) is a subject of debate. Smith (1991, 1992) concludes that a glue-like adhesion is responsible for the great tenacities observed in limpets by Grenon and Walker (1981) and Denny (1984), although whether this glue is related to, or is part of, mucus is not clear. It may be that these tenacities are is not a product of a glue or mucus at all, but are owing to a very flexible muscular foot which can effectively mirror, and hence grip, the microscale contours of substrata. This would explain the way in which limpets can increase their tenacity when disturbed. Davies and Case (1997) who studied the tenacity of two littorinid species, concluded that “muscular grip” does not play a role in adhesion. They suggested that the mechanism of adhesion in these animals involves mucus. Grenon and Walker (1982) measured the thickness (3 μm) of the mucus layer under the foot of Patella vulgata after it had been attaching to an alga for 2 d. Grenon and Walker suggested that adhesion was afforded by the thinness of the layer (cf. Branch and Marsh, 1978) caused by the slow uptake of water and mucus from the sole of the foot by epithelial cells, a mechanism proposed by Zylstra (1972) and Machin (1975).
Cephalopods also use mucus in escape from predators. Their “ink”, squirted at predators to confuse them is bound with mucus to prevent its rapid dispersion in water (Denny, 1989).