Greener obscurer (or Why does mud stick?)

The land snail Merdigera obscura (Muller, 1774) is of interest because frequently it can be found with the shell covered in material from its environment. Occurring more often in juveniles, this coating can appear to be of mud, soil particles or small fragments of lichen. The shell may be part coated or not coated at all. Why?

Superficially these coatings can, to our eyes at least, make the animal well camouflaged (Figs. 1 to 4). This feature of M. obscura has been known since at least the early 19th century, being described by the Rev. R. Sheppard as follows: “These shells, particularly in their young state, show great sagacity and ingenuity by covering themselves with an epidermis adapted to the situations in which they are found; and when so covered, it is almost impossible for any other than a conchological eye to detect them. If its abode be upon the trunk of a tree covered with Lichens, then is the epidermis so constructed as to cause the shell to resemble a little knot on the bark covered with such substances. If on a smooth tree, from whose bark issue small sessile buds, as is frequently the case, it will pass off very well for one of them; and on a dry bank, or the lower part of the body of a tree splashed with mud, its appearance will be that of a little misshapen, pointed piece of dirt.” (Sheppard, 1825). Subsequently, other 19th century authors made interesting additional comments, for example, “sometimes the disguise, instead of being formed of mud, consists of minute lichens, the spores of which have fallen upon and taken root in the epidermis of the shell.” (Rimmer, 1880). Later, Adams (1896) added “In some districts where the foreign matter is not suitable for attachment (as in the calcareous districts of Derbyshire), the shell is found clean and smooth in the crevices of rocks.” Finally, Step (1901) provided an alternative description as to how this coating is achieved: “It is an inactive creature, sticking on the bark of trees (beech chiefly) apparently feeding upon the immature mosses and lichens that grow thereon, and disguising itself so that snailhunting birds may pass it as a bit of dirt or one of the small knots that are so common on tree bark. It does this by covering its shell with slime and dragging it across dirt of various kinds which gets picked up by the slime. The process several times repeated, the shell soon bears no resemblance to itself.” Step does not claim first hand experience of observing this behaviour but neither does he refer to it as the observation of another field naturalist. These descriptions as to how the coating is achieved are somewhat at variance with one another but are not necessarily mutually exclusive (nor indeed with the literal meaning of its scientific name Merdigera obscura; “the hidden excrement bearer”!).

Whether this is an active piece of behaviour or a more passive process, the phenomenon raises a host of questions. Why are some individuals coated and others not? Why is it apparently more common in juveniles? Why does the nature of the material used vary? If acquisition of the shell covering is an active process then what environmental cue, if any, triggers it? Is it safe to assume that its adaptive significance really is to provide camouflage? The answer to the last question may seem obvious but care should be taken not to make assumptions in the absence of reliable evidence and perhaps other explanations should be given at least some consideration. If the shell covering is an anti-predator adaptation, providing camouflage, then M. obscura should have one or more predators that have vision similar to ours and that hunt primarily by sight. As it frequently ascends and rests exposed on tree trunks, vertical rocks and walls it is here that one might expect M. obscura to be subject to predation, perhaps by bird species that forage in such places. However, colour vision and perception in birds does differ from that of mammals so the assumption that they see what we see should not be taken for granted (Goldsmith, 2006). If candidate species could be identified as possible predators then the next step might be to demonstrate reliably the selective advantage of the shell covering as camouflage in natural conditions, something which undoubtedly would be very difficult, as comparable studies in the past have shown. Extensive studies by Kettlewell in the 1950s attempting to demonstrate the selective advantage of industrial melanism in the Peppered Moth (Biston betularia) come to mind, together with subsequent debate about the validity of the results; see Hooper (2002) for references to Kettlewell’s original papers and a critique. With respect to land snails the classic studies of selective predation by the Song Thrush (Turdus philomelos) in maintaining balanced polymorphism in Cepaea nemoralis have been extensive and are well known but, interestingly, there seem to be several other additional forces at play (Jones, 1977).

Returning to M. obscura, in a case such as this there is always the possibility that in its present day habitats the shell covering is redundant as an adaptive feature and that it evolved as a result of selection by a visual predator that is no longer present or no longer present in sufficient numbers to exert a detectable selective pressure. Such evolutionary “lag” is a well known phenomenon, occurring for example in the adaptation of several Costa Rican plants to fruit dispersal by large mammals such as the gomphotheres, which have been extinct for 10,000 years (Ridley, 1993). Finally, it should be borne in mind that simply because shell covering disguises M. obscura to the human eye this is not necessarily the reason for it. Other possibilities, whatever their degrees of likelihood, are numerous. For example, the covering could act as a tactile camouflage or olfactory or gustatory camouflage against predators that hunt over its 21 habitat primarily by sense of touch or use of chemoreceptors; one might speculate on a beetle species as a possible candidate. Alternatively the covering may serve some entirely different purpose for example thermal stabilisation or reduction of desiccation when the animal rests in an exposed position, with an apparent visual camouflage effect being an incidental but inevitable consequence of the animal utilising local material. These alternative suggestions are not necessarily mutually exclusive nor are they an exhaustive list.

Rievaulx Terrace, North Yorkshire (NZ5784) is a good place to observe M. obscura resting in tree trunks by day, the trees present being young beech, ash and sycamore of at present about 0.3m diameter at height 1.5m. A variety of other mollusc species can be seen here, either active or resting, at different times and in particular weather conditions. These include Lehmannia marginata, Cochlodina laminata, Clausilia bidentata, Trochulus striolatus and Cepaea hortensis; also occasionally Arion subfuscus and Arianta arbustorum. Of these, why is M. obscura the only snail species to have a shell covering? Some of the others, such as C. hortensis, are decidedly conspicuous and, one might think, vulnerable to predators. Against this background a recent article in the Journal of Conchology by Yanes et al. (2010) was of particular interest. This deals with three Canary Island species of Enidae, the family to which M. obscura belongs. Napaeus barquini, a rock dwelling species has been observed to cover its shell with fragments of lichen, grazed and adhered by mouth, forming protuberances and reminiscent of Figure 1 of M. obscura. In contrast, the ground dwelling Napaeus variatus develops a covering of mud passively; it simply seems to get dirty. A third species, N. badiosus, which was the main subject of their study, does not have a covering on its shell and normally rests out of sight under stones or in rock crevices. Four specimens of this species were placed in a terrarium containing soil but no suitable places for the snails to hide. During the night of their transfer to the terrarium they actively used the soil to cover the surface of their shells, resulting in an appearance similar to that of N. barquini. The authors interpret this behaviour as being adopted when hiding places are not available and presume that it reduces the risk of visual predation. They cite a lizard, Gallotia atlantica, known to feed on these snails, and also the song thrush, as possible selective agents favouring visual camouflage.

Yanes et al. (2010) did not speculate on what environmental cue might trigger (or inhibit) active covering of the shell, notably in N. badiosus, an aspect of this behaviour which could be a separate issue from its adaptive advantage. For example, the adaptive advantage may be visual camouflage but the environmental cue for what is surely an innate piece of behaviour is not going to be conscious awareness of exposure and anxiety about possible predation! Several other, albeit less likely, adaptive advantages were considered earlier and possible environmental cues are equally numerous. For example, in an exposed environment this could be a response to lower humidity or higher temperature resulting in dehydration, to a period of exposure to higher light intensity or continuous exposure to light or to thigmokinesis (failure to locate a suitable crevice and the tactile stimulus it provides). It may be, of course, that not all species which exhibit active shell coating respond to the same cue and in some (those which apparently always coat the shell) it could be purely innate with no environmental cue needed.

Yanes et al. (2010) refer to some other recent descriptions of shell covering, mostly in species of Enidae, but not to M. obscura and the older references noted above nor to the two other British species that exhibit this behaviour, Ena montana and Abida secale. The fact that this behaviour occurs in several species of Enidae, collectively with a fairly wide geographical distribution, suggests that it has a long evolutionary history, longer than the life of individual species or even genera, unless it has evolved independently in more than one lineage. A parallel situation exists in the case of balanced polymorphism in shell colour and banding pattern in Cepaea species and related genera.

Of the two other British species which develop shell coatings Rimmer (1880) made the following statements, “The young of … B. montanus [= Ena montana] as well as those of Pupa secale [= Abida secale] are often similarly encrusted with mud.” and of E. montana, “In spring this snail ascends trees (especially the beech) to a considerable height; it should consequently be searched for in early spring before it has made its ascent, or in autumn when it descends to seek its winter quarters.” Thus shell coating in E. montana, and possibly M. obscura, may tie in with life cycle, young individuals developing it and older individuals sometimes losing it again through wear and tear when they return to ground level.

Some of the ideas in this article are intentionally speculative. Hopefully they will serve to show how much scope there is for further investigation in order to develop a fuller understanding of this fascinating aspect of molluscan behaviour.

References:

Adams, L. E. (1896) The Collector’s Manual of British Land and Freshwater Shells.Taylor Brothers, Leeds.

Goldsmith, T.H. (2006) What birds see. Scientific American: 69-75.

Hooper, J. (2002) Of Moths and Men. Fourth Estate, London. Jones, J. S., Leith, B. & Rawlings, P. (1977). Polymorphism in Cepaea: a problem with too many solutions? Ann. Rev. Ecol. System. 8: 109-143.

Ridley, M. (1993) Evolution. Blackwell, London. Pp. 333-334.

Rimmer, R. (1880) The Land and Freshwater Shells of the British Isles. John Grant, Edinburgh.

Sheppard, R. (1825) Description of Seven new British Land and Freshwater Shells,with Observations upon many other species. Trans. Linn. Soc. Lond. XIV: 148-170.

Step, E. (1901) Shell Life. F. Warne, London.

Yanes, Y., Martin, J., Delgado, J. D., Alonso, M.R. & Ibanez, M. (2010) Active disguise in land snails: Napaeus badiosus (Gastropoda, Pulmonata, Enidae) from the Canary Islands. Journal of Conchology 40: 143-148.

figures 1-3 (left to right): Merdigera obscura with shell coated or part coated in lichen fragments, taken 31.10. 2009, Rievaulx Terrace, North Yorks. (photo figure.1: M. Wardhaugh)

figure 4: M. obscura, Rievaulx Terrace.