Tuatara: Volume 25, Issue 2, January 1982
How to Be Sluggish
How to Be Sluggish
Being a soft-bodied, succulent, fleshy water bag in a dry environment poses problems, which range from simply drying out, through being stepped on, to being leapt on with greed by some heartless predator. On the face of it, a land mollusc seems a highly unlikely proposition, but the terrestrial molluscs have evolved satisfactory answers to the daunting array of potential disaster which confronts them, and have done it so successfully that they can be found in large numbers in an extraordinary variety of habitats all over the world. These habitats do not include only the moist areas; snails are common in many arid areas, and can be spectacularly successful in withstanding desiccation. A famous example is that of a specimen of the South African desert snail Eremina desertorum, glued to a card in the British Museum in 1846, which emerged from its shell and happily crawled off into the middle distance when exposed to moisture four years later. This ability to wait through dry conditions has often been noted — the West Australian camaenid snails are good at it, as are the South Australian helicellids, many African helicidae, and the prosobranch land snails of the Khasi Hills of Assam. Many deserts of the world have their populations of land snails, all waiting patiently for the rains to come.
The ability to retain water is the key factor for a snail living on land. Snails are inveterate hypochondriacs, constantly fretting about their water balance, and modifying their entire life style to keep that balance within allowable limits. Obviously, there are basic structural adaptations involved, but modifications to behaviour patterns, such as a nocturnal habit, the ability to seek out moist micro-habitats, and the ability to aestivate are also important (Hyman, 1967; Solem, 1978). This paper, then, will look at the hazards faced by the land molluscs, the modifications which allow them to deal with those hazards, the selective presures which have influenced the development of the slug form, and the evolution of one group of slugs in particular, the Athoracophoridae.
The Class Gastropoda is divided into three subclasses, the Opisthobranchia, Prosobranchia, and Pulmonata; the prosobranchs and pulmonates both have land representatives. The prosobranchs retain the open mantle cavity found in marine forms, and when they retreat into the shell during dry conditions they seal the opening with an operculum. As a water retention device, this is superb; in fact the seal is so effective that accessory notches, slits, grooves or separate tubes have evolved to allow air to circulate past the barrier of the operculum (Rees, 1964). However, the arrangement of the prosobranch mantle cavity allows high rates of water loss when the snail emerges, unless conditions are very humid. In the land prosobranch, the gills are lost and respiration takes place on the inner surface of the mantle. The kidney secretes a stream of almost pure water from the posterior of the pallial cavity, and this moistens the cavity, allows respiration, and stops the tissues drying out — at a cost. The arrangement is only marginally efficient. The snail can be active in periods of very high humidity, but when ground level humidity drops below about 95 per cent, the snail must retreat behind its operculum and wait for wet weather to return. This obviously cuts down the opportunities the snail has for feeding and mating.
The pulmonate snails lack an operculum to seal the shell aperture. Instead they secrete an epiphragm, a membrane of mucus or calcified page 49 mucus which may prevent water loss just as effectively as an operculum, but which still allows air to filter back and forth. Thus pulmonates can withstand dry conditions just as well as prosobranchs, but it is when humidity falls that pulmonates have the edge. They gain this edge through a number of modifications.
First, the pallial cavity, instead of being open, is enclosed, and the mantle collar is fused to the neck of the snail. This creates a large internal chamber communicating with the outside through a pneumostome, and this allows water loss over the breathing surface to be controlled. A bonus is the ability to retain reserve water inside the mantle cavity; this reserve may be as much as one-twelfth the total body weight (Blinn, 1964). Having a savings account of water allows a much more flexible approach to changing conditions. A pulmonate can remain active when a prosobranch is forced by falling humidity to withdraw into its shell, and this enables the pulmonates to exploit a wider variety of habitats.
Second, the pulmonates have evolved various methods of reducing water loss during excretion and respiration. A new organ, a ureteric groove or tube, develops in pulmonates, and there is direct evidence that in some species at least water resorption from kidney filtrate does take place (Vorwohl, 1961; Martin et. al. 1965). In many pulmonates, the kidney opens inside the pallial cavity some distance away from the pneumostome, and the excretion products must then be flushed out. In the order Sigmurethra there are various combinations of ciliated grooves and-or closed tubes that arise from the kidney, pass posteriorly to the hindgut, then reflect forward and continue partway to or actually reach the pneumostome. The evolution of this tube permits water conservation, and having it exit direct to the exterior through the pneumostome means that excretory products can be got rid of without having to use extra water to flush them out of the pallial cavity. (Solem, 1978).
Third, the pulmonates are well equipped to make good use of the water which they have. The physiological mechanisms which allow this are revealed in the relative impermeability of the mantle collar to water (Machin, 1966), and in the ability to withstand considerable water loss over long periods of time. Helix can survive water loss of around 50 per cent body weight, Arion 60 to 66 per cent, and Limax 75 to 80 per cent. In such a desiccated state Helix can survive 10 to 11 months, and Helicella over a year (Hyman, 1967).
Fourth, an array of other modifications also comes into play in resisting desiccation. These include the development of retractable tentacles, and the use of slime to cut down evaporation from moist surfaces.
Superimposed on all these structural modifications are behaviour patterns which cumulatively reduce the effects of desiccation and predation. A generally nocturnal life style, retirement to crevices in dry conditions, aestivation, burrowing (in slugs), and withdrawal into the shell during periods of lowered humidity are all effective. Taken together, this battery of adaptations and behaviour patterns has given the molluscs major successes in conquering the land.
The Qualifications for Slugdom
A slug is any snail in which the shell is completely lost, or buried in the mantle. If land snails are an unlikely proposition, then slugs seem doubly unlikely — but there are some 500 species of terrestrial slugs, and approximately 1000 species of land-dwelling “semi-slugs” in which the shell has become reduced to the point where the animal cannot withdraw page 50 fully into it. There is no doubt that a shell is a very useful attribute for a large number of land molluscs, but it is also clear that there are powerful selective forces that influence land molluscs to reduce and finally lose their shells.
It has been known for over a century that all land slugs are not closely related, but have evolved independently from several different snail groups. These groups are not randomly distributed among the land snails. Solem (1974) recognises 60 families of land snails divided into six orders. Two of these orders, the Onchidiacea and Soleolifera, contain nothing but slugs. Animals in these orders show many peculiarities in structure and their relationships with other land snails are uncertain. All other slugs are found in the Order Sigmurethra, which contain a mixture of shelled, semi-slug, and sluglike species. Even here, the distribution of slugs is not random. Of the 14 families making up the Suborder Holopodopes, there is only one family of slugs, the Aperidae, and two families of semi-slugs, the Rhytididae and Bulimulidae. Of the 10 families constituting the Order Holopoda, only the Helminthoglyptidae contain semi-slugs. In contrast, 18 families comprise the Order Aulacopoda. Five of these, the Philomycidae, Parmacellidae, Limacidae, Testacellidae, and Athoracophoridae, contain only slugs; one, the Arionidae, contains only slugs and semi-slugs; two, the Helicarionidae and Urocyclidae, possess shelled, semi-slug, and slug species in great variety, and a further three, the Charopidae, Succineidae and Zonitidae, have mainly shelled and a few semi-slug species. The remaining seven of the 18 families contain only shelled forms. The Orders Orthurethra and Mesurethra contain no slugs (Runham and Hunter, 1970). In both these groups the excretion products are released well within the pallial cavity and are subsequently flushed out, and there is no water-resorbing ureter (Solem, 1978). The pallial region, then, provides one of the major clues to why slug evolution is restricted to a few groups of land snails. All slugs have a long, closed ureter opening directly to the outside, thus allowing resorption of water from kidney products, and avoiding the expense of flushing those products from the mantle cavity. Slugs and semi-slugs have evolved only in the Superorders Sigmurethra and Systellommatophora, the two major groups with a closed ureter. Probably the existence of a water-conserving ureter was a preadaptation for the evolution of slugs.
What, then, are the selection pressures which favoured reduction of the shell in so many pulmonate families? First, slugs are common in those areas where microhabitats with plenty of moisture exist. Such a microhabitat, which maintains high levels of humidity through the year, means that a shell is no longer so vital. Second, a shell requires calcium. This tends to preclude snails from calcium-deficient areas. Third, building, transporting, and maintaining a shell requires energy. Fourth, a bulky shell prevents a snail from getting into crevices, which may make it difficult for it to avoid both desiccation and predation. These factors in combination are quite sufficent to allow a slow reduction in shell size where conditions are right and in those groups which possess adequate water conservation mechanisms.
Of course, the loss of the shell does mean that slugs are more likely than snails to be eaten by something large and unfriendly. However, they have developed other defences. Many of the Arionidae are brightly coloured — and distasteful. The Athoracophoridae in particular have developed cryptic colouration to a high degree. The pattern of grooves they show on the back closely resembles the veins of a leaf, and Athoracophorus page 51 bitentaculatus shows a range of colour patterns which mimic the colour changes which occur in fallen leaves, from yellowish-green through to chocolate brown, all in the same population. One variety of the Australian athoracophorid Triboniophorus graeffei is much the same size and colour as half a saveloy — a bright, fire-engine red which precisely matches the colour of fallen leaves in the area (J. B. Burch, pers, comm.). Other defences are warts, bumps, papillae, and the secretion of large quantities of distasteful slime when attacked. Moreover, the development of the slug form allows slugs to burrow into the soil, or get into crevices, or, in some of the Athoracophoridae, to get right inside rotting logs where they are protected from predatory birds and have a secure food source.
The Path to Slugdom
|p.r.m.||penis retractor muscle|
|Scale divisions in mm|
Sluggishness in the Athoracophoridae
The Athoracophoridae are a family of slugs found in New Guinea, eastern Australia, the Bismarck Archipelago, the Admiralty Islands, the New Hebrides, New Caledonia, New Zealand, and the subantarctic page 55 islands. They have always been considered aberrant, and regarded with deep suspicion by a number of malacologists, but recent work on the group (Burton, 1977, 1978, 1980, 1981a, 1981b in press; Barker 1978) has led to a reversal of many previous ideas, and it is now possible to assess the group in the light of the processes involved in slug evolution outlined above.
The family comprises two subfamilies, the northern Aneiteinae and the New Zealand and subantarctic Athoracophorinae, and contains only slugs — no semi-slugs or snails need apply. The shell is reduced to a number of calcareous deposits embedded in the remains of the mantle collar, and in many specimens even these are missing. There is no sign of a visceral hump, and the pallial complex has become flattened and compacted to a high degree, with a highly convoluted and elongated ureter and a compact, high-surface-area lung of a type found in no other mollusc. There is no question that the Athoracophoridae as a group have advanced far down the road to slugdom. Obviously, there can be no fossil evidence to show the details of the path they have taken, and all the clues must be gleaned from a study of comparative anatomy. Nevertheless, the Athoracophoridae are a varied group, and a close study reveals that the clues are plentiful. The New Zealand and subantarctic species in particular show a rich web of inter-relationships and a gradation of answers to specific problems. The conceptual tool which allows fruitful exploration of the problems posed by the Athoracophoridae is Solem's work on the effects of compaction (Solem, 1966, 1972, 1974, 1978).
Fig. 5 Pallial complex of Athoracophorus bitentaculatus, exploted view. Drawn from serial sections. Not to scale.
Fig. 7 Changes associated with flattening in the Athoracophoridae. The representative chosen as the starting point is Triboniophorus graeffei.
Similarly, taking the compaction hypothesis into account, some evolutionary trends could be inferred in the reproductive systems of the diaulic Athoracophorinae. Such trends include the development of a discrete prostate and a distinct oviducal gland, and a general shortening of the reproductive tract (Fig. 10). It must be stressed that this figure does not imply an evolutionary relationship between the species named; each species simply illustrates a different stage in a possible evolutionary sequence.
Thus the process of compaction has been carried almost to an extreme in the Athoracophoridae, and in Athoracophorus bitentaculatus in particular. In this species it has resulted in a slug so flattened that it can easily fit into small crevices and spaces between leaves denied to fatter slugs, and thus gain protection from desiccation and predation. Second, compaction and flattening confers on the slug a much higher foot area-weight ratio, which improves its ability to climb up vertical surfaces and allows it to browse on trunks and leaves at night.
The Athoracophoridae as a group are highly advanced in some respects. Solem (1974) has described slugs in general as representing the acme of land snail evolution. As Athoracophorus bitentaculatus in particular has carried the process of compaction to its logical extreme, it can be regarded as a supreme example of the current state of the art in the land mollusca.
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