Skrjabingylosis

Museum curators and researchers dealing with collections of weasel skulls noticed long ago that many specimens were damaged in the postorbital region, immediately behind the eyes. The skulls had what appeared to be dark patches or swellings with thinned walls, and sometimes these had holes in them, even large openings (Figure 11.7).

The cause of the damage became clear when the fresh heads were skinned and the swellings opened. Inside, a mass of bright red round worms could be seen crammed into the tiny sinuses in the nasal bone, coiled over each other and pressing hard against the confining skull. The worms were described in 1842 by Leuckart, and are now known by the tongue-twisting name of Skrjabingylus nasicola—after Skrjabin, the great Russian parasitologist, and "nasicola" because of their position. The condition of being infested with these worms is called skrjabingylosis.

These parasites have attracted a lot of attention, for two reasons. First, they are easy to observe in freshly dead mustelids, where they are very dramatic in appearance. Better still, their effects can be studied indirectly from standard museum material. A large collection of skulls allows the incidence and geographical distribution of damage to be calculated with minimum effort. The cheap and simple technique of visual inspection of preexisting material has ensured many more studies of the damage caused by skrjabingylosis than of the parasite itself. Fortunately, the link between the visible damage and the incidence of infestation is secure (Lewis 1978).

Second, there is the economic aspect. In the far north, weasel furs were once a valuable item of trade, and most of the earliest research on skrjabingylosis was concerned with the effect of the disease on the harvest. Looking at an advanced

Figure 11.7 The skulls of weasels commonly show more or less severe distortions and perforations in the postorbital area caused by Skrjabingylus worms, and their severity generally increases with age (shown left to right). (Redrawn from King 1977.)

case, it is hard to avoid the impression that such severe distortion of the skull bones, and consequent pressure on the brain (Figure 11.8), must have some effect on the general health of the afflicted animal, possibly a fatal one. Hence, in the early 1940s Russian biologists interpreted their data to mean that stoats heavily infested with S. nasicola were in poorer condition, were less fertile, and died sooner than uninfested ones, and that the fur harvest was lower in seasons following widespread infestations (Popov 1943; Lavrov 1944).

Conversely, there are other places where any species of weasel is regarded as a pest. People concerned with the protection of birds, usually game or endangered native species (Chapters 12 and 13), would welcome any prospect of biological control of weasel populations using a specific and fatal parasite, and encourage research on means of spreading it (McDonald & Lariviere 2001).

Common Weasel
Figure 11.8 The head of a common weasel cut in cross section in the postorbital region. (1) Skrjabingylus worms; (2) brain; (3) muscles; (4) skull (to the left of the arrow, the zygomatic arch or cheek bone; to the right, the cranium). (From King 1977.)

The proportion of skulls visibly damaged by skrjabingylosis is not quite the same as the incidence of the disease in a population, since very early infestations are not detected this way. Nevertheless, damage does closely reflect both incidence and severity (the number of worms in each skull). Studies of damaged skulls in museums, therefore, give an idea of local and regional variation in incidence (Table 11.8).

These general figures are not very informative, however. Estimates of incidence are strongly affected by sampling variables, such as the season of collection and the age structure of the target population, and the incidence in any one area may vary from year to year (King 1977; Weber 1986). Moreover, since the worms tend to damage smaller skulls more severely, the disease is probably detected at an earlier stage in females than in males of any species, and more often in common and least weasels than in stoats and longtails. Consequently, estimates of damage are not strictly comparable in skulls of different sizes.

The biology of the parasite was worked out in the laboratory by Dubnitskii (1956). Male and female adult worms are easily distinguished from their size; the females measure 18 to 25 mm long, with a diameter of 0.8 mm, and the males about 8 to 13 mm by 0.5 mm. The first-stage larvae, about 300 mm long, travel from the sinuses down the nasal passages to the back of the throat. From there they pass into the gut and to the outside with the feces. They actively disperse onto nearby grass and leaves, and await their opportunity to invade the soft foot tissues of a slug or a snail.

After 12 to 18 days in a slug or snail, the larvae pass through an obligatory intermediate second stage. When they reach a weasel, the third-stage larvae (now grown to 700 to 750 mm long) pass from the gut into the tissues, through two more

Table 11.8 Regional Variation in Incidence of Skrjabingylus nasicola in Weasels1

Species

Country

Incidence

References

Stoat

Britain

17-30%

(Lewis 1967; van Soest et al. 1972)

Eurasia

20-50%

(Lavrov 1944; Vik 1955; Hansson 1970; van Soest et al. 1972; Debrot & Mermod 1981; Sleeman 1988b)

North America

20-100%

(Dougherty & Hall 1955)

New Zealand

0-40%

(King & Moody 1982)

Common and

Britain

70-100%

(King 1977)

least weasels

Eurasia

20-60%

(Lavrov 1944; Vik 1955; Hansson 1970; van Soest et al. 1972)

Longtail

North America

0-100%

(Dougherty & Hall 1955)

Manitoba

100%

(Gamble & Riewe 1982)

1. Ranges of mean incidences given refer to different localities.

1. Ranges of mean incidences given refer to different localities.

molts, and then migrate to the nasal sinuses along the spinal cord as fifth-stage larvae. They grow to adult size and settle in, wriggling around in the confined space and gradually enlarging it.

How they cause the swellings and perforations we see is not quite clear. Simple friction, the rubbing of the worms' hard cuticle against the sensitive bone tissue, could cause the enlargement or, possibly, the worms produce some kind of corrosive agent that interferes with the control of the living bone tissue or erodes it directly. Damage often increases with weasel age, which suggests repeated reinvasions.

The main problem faced by the larvae is how to get from the snail to a weasel. Weasels do not eat snails or, at least, not nearly often enough to account for the high frequency of infestation in some places. Other animals do eat snails regularly, for example, many of the shrews. A larva finding itself inside a shrew will simply retreat into a cyst and wait. The shrew is not needed as part of the parasite's life cycle, but it can act as a paratenic (waiting) host, a bridge to the definitive host where the larvae can complete their development into breeding adult worms.

If an infected paratenic host is eaten by a weasel, the cyst opens in the weasel's gut and the larva continues on its interrupted journey. Hansson (1967) showed that it was possible to transmit skrjabingylosis into a previously uninfested weasel by feeding it shrews. The suggestion that shrews might be a natural paratenic host was strengthened by the fact that incidence rates are particularly high in places where weasels eat shrews more often than usual.

For example, on Terschelling Island, off the coast of the Netherlands, the incidence rate observed by van Soest et al. (1972) was over 90%, much greater than on the nearby mainland coast (23%). As Terschelling has no voles, stoats there had to eat a lot of shrews. North American stoats, too, tend to eat shrews more often than do their European brethren, and they also suffer a generally higher rate of infestation. In western Newfoundland, the incidence of skrjabingylosis in stoats increased dramatically after shrews were introduced to the island (Jennings et al. 1982).

In most places, however, weasels do not normally eat shrews often enough to explain the high incidence of skrjabingylosis. Hansson's experimental animals ate shrews only with the greatest reluctance. Besides, a few weasels in Newfoundland had skrjabingylosis before the shrews arrived, and there are no shrews in New Zealand, where the parasite arrived with its hosts and has persisted for a hundred years (King & Moody 1982).

The solution to the mystery was found by a doctoral student at Neuchatel and published in two joint papers with his supervisor (Weber & Mermod 1983, 1985). Weber discovered encysted third-stage larvae in the salivary and lacrimal glands of wood mice and bank voles, and also in the muscles and connective tissues of their heads. These small rodents, especially wood mice, do eat slugs and snails occasionally (Figure 11.9), not as a main item of diet, but often enough when green food is scarce in late winter that some become carriers of invasive larvae (the strictly vegetarian field vole would rather starve).

Weber fed infected rodents to one common weasel and one stoat, plus six ferrets that were bred in his laboratory and known to be free of the disease. He checked every day for the development of the adult parasites by inspecting the mustelids' scats in water under a binocular microscope. A host carrying both sexes of worms in the same sinus passes a continual stream of first-stage larvae, which can easily be seen swimming about in the water.

Within 30 days, the common weasel, the stoat, and three of the ferrets were infected. Those that had been given whole rodents or only the heads and front ends produced larvae first; one ferret given the hind end produced larvae only much later; and three ferrets given only the viscera (heart, lungs, liver, intestine) remained free. It is a fact that weasels usually begin to eat their prey at the front end (see Figure 2.5), and may leave the viscera. Hence, the larvae not only seem to choose a paratenic host frequently eaten by weasels, but they are also most likely to encyst in the part of the body first eaten by a weasel.

Parasites often show such remarkably close adaptations to the feeding habits of their definitive hosts, for the simple reason that their lives depend on it.

Figure 11.9 The life cycle of Skrjabingylus nasicola in weasels. (a) First-stage larvae leave the weasel in the scats. (b) The larvae have to pass through the next two molts in a compulsory intermediate host, a mollusk. (c) Third-stage larvae encysted in the mollusk tissues can reach a weasel directly, but this is rare as weasels seldom eat mollusks. (d) Usually the larvae make use of a paratenic host, a shrew or a mouse that has eaten an infected mollusk. (e) On being eaten by a weasel, the larvae escape from their cysts, pass through another molt, and migrate to the nasal sinuses along the spinal cord. (Redrawn after Weber 1986.)

Figure 11.9 The life cycle of Skrjabingylus nasicola in weasels. (a) First-stage larvae leave the weasel in the scats. (b) The larvae have to pass through the next two molts in a compulsory intermediate host, a mollusk. (c) Third-stage larvae encysted in the mollusk tissues can reach a weasel directly, but this is rare as weasels seldom eat mollusks. (d) Usually the larvae make use of a paratenic host, a shrew or a mouse that has eaten an infected mollusk. (e) On being eaten by a weasel, the larvae escape from their cysts, pass through another molt, and migrate to the nasal sinuses along the spinal cord. (Redrawn after Weber 1986.)

Nevertheless, the parasitic way of life is hazardous. Weber calculated that, of every 100 first-stage larvae given the chance to invade a slug, only about 24 reached the infectious third stage, and only six became adult worms (Weber & Mermod 1985).

The losses during the life cycle of the parasite are high even in the ideal conditions in the laboratory; in the wild, they are much worse. In Weber's study area at the time of his observations, the infestation rate in stoats was 11%, but only two (0.3%) of 762 molluscs and two (4%) of 48 shrews and small rodents he examined were carrying larvae. The system is wasteful, but it works because the number of larvae produced is so enormous, because small rodents are so frequently eaten by weasels, and because the time the larvae are prepared to wait in a rodent is so long (at least a year).

Geography and climate also play their part in determining incidence. The disease is generally more prevalent in damper habitats, and absent in deserts. The reason is mainly to do with the conditions that favor the survival of the free larvae and their chances of making the hazardous journey from the weasel's scats to a mollusk's foot. The larvae are very susceptible to drying, and to freezing when they are swimming in water (Hansson 1974). The best conditions, both for the larvae and for the mollusks, are found in a mild and humid climate. In different districts of Sweden and Britain (Table 11.8), the frequency of incidence of the disease or the severity of damage it causes increases with the number of rainy days per year.

Strangely, the opposite correlation was observed in New Zealand. In the wettest places sampled, all with mean annual rainfall over 3,000 mm, the incidence of skrjabingylosis in stoats was 0% to 7%, whereas higher local incidences (15% to 60%) were found only where rainfall was under 1,600 mm. This contradiction was completely inexplicable at the time it was published (King & Moody 1982). Since then, however, Weber's demonstration of the role played by wood mice in the transmission of the disease in Europe has suggested a possible solution to the puzzle.

Feral house mice are generally less common in the wetter western mixed podocarp forests of New Zealand, where incidence of skrjabingylosis was low, than in the dryer eastern beech forests and grasslands where incidence was higher. If these mice are the paratenic host transmitting skrjabingylosis to New Zealand stoats, then individual stoats that have passed their whole lives in the period between postseedfall mouse irruptions should be less likely to have picked up the infection than stoats that were born in or lived through a mouse irruption. King (1991c) returned to the original data, and found some support for this hypothesis, especially in females (they eat mice more often than males; Chapter 5). Hence, geographical variation in the relative density of feral house mice could explain the unexpected distribution of skrjabingylosis in New Zealand.

Much work on skrjabingylosis has been done since the early Russian studies that claimed a detrimental effect on infested individuals. When van Soest et al. (1972) measured a sample of stoats from Terschelling Island and found them to be a little smaller in general than those on the mainland, they wondered if the island animals were stunted by the high rate of infestation they suffered. To be valid, such a comparison must be made only between infested and clean individuals of the same age and sex living under the same conditions. Whenever this has been done, there has been no sign that the infested animals were any smaller, were any lighter or leaner, or died sooner, than the others (King 1977; King & Moody 1982).

On the other hand, incidence of skrjabingylosis in Russia and in Switzerland does increase after a population crash. Early writers attributed the decrease in weasel numbers to the increased infestation, but Debrot and Mermod (1981) suggested that the relationship works the other way around. In both countries, stoats reach a high density when water voles are abundant (Chapter 10). Water voles are strictly herbivorous, and are not at all implicated in the transmission of skrjabingylosis. When water voles are abundant, stoats eat them almost exclusively and run little risk of picking up the parasite. When water voles decrease in numbers, however, stoat numbers also decrease and the survivors are forced to turn to alternative prey, including wood mice, which are the most likely of the other rodents to be carrying invasive larvae.

Hence, Debrot documented an increase in infestation during the population decline in the Brevine valley, from 4% when the stoats were feeding almost exclusively on water voles to 50% after the forced change of diet. This attractive idea was confirmed in the Val de Ruz by Weber (1986). Unfortunately, no one seems to have thought of the possible effect on these figures of the change in age structure, which also follows a population decline. The higher proportion of older stoats in the postpeak population would, in itself, cause an increase in incidence, since incidence increases with age and weasels have practically no resistance to infestation and no means of repairing the damage (Lewis 1978). Debrot's hypothesis should be tested; in the meantime, the role of skrjabingylosis in the population dynamics of weasels remains unknown.

Even if S. nasicola has no effect on populations, it could still affect the behavior of individuals. The pressure on the brain caused by the distortion of the skull, plus the wriggling of the worms, must be intensely irritating. Weasels observed behaving strangely in the wild, leaping about and somersaulting, are said to be "dancing," either in play or as a clever trick to catch birds (Chapter 6). They are also believed to suffer "fits," or to "play dead" after violent exertion (Chapter 8). Perhaps these gyrations and temporary blackouts are merely an understandable response to the extreme discomfort caused by having to carry such unwelcome and relatively enormous guests in the head. At present, we do not know one way or the other.

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