Responses Of Voles To Weasels

The vole that can avoid becoming weasel food for longest has the best chance of leaving surviving offspring. A vole that makes a bad move, and ends up moving through a weasel gut rather than through its own tunnel system, has less or no chance of contributing to the next generation. In the relentless calculations of evolution, natural selection favors the family prospects of voles that maintain constant vigilance for predators. (We refer here to voles because much of the research on this subject has been done on voles; other small mammals may behave similarly.)

Voles appear to respond to the presence of weasels and other predators on at least two different levels. One is the level of immediate, deliberate behavior: Stop, look, listen, and "lay low" (Jgdrzejwski et al. 1992, 1993; Borowski 1998). These responses clearly benefit the individual vole that escapes a weasel for one more day. The second is the level of long-term, unconscious effects. Perhaps cautious behavior and stress induced by the prolonged presence of danger may inhibit the feeding rate and reproductive success of voles (Ylonen 1989). Both these responses have costs. The vole that lives but fails to reproduce contributes no more genes into future generations than does the vole that fails to avoid being eaten by a weasel.

When a vole detects a weasel entering its runway or nest, it skedaddles (Jgdrzejwski et al. 1992). Flushed voles will run in the open if necessary, but they attempt to escape into thick vegetation or under dead leaves as soon as possible. Presumably, their best bet is to dive for a known hole for shelter, though they will climb twigs or sturdy, herbaceous vegetation if closely pursued. On the other hand, that strategy can quickly give away its position to a weasel that spots move ments more quickly than motionless shapes. So, if it finds a relatively safe place, a vole (or, especially, a mouse) will freeze. Because the eyes of weasels are especially alert to detect movements, a small rodent sitting stock still but in plain view has a chance of melting into the background for long enough to avoid notice.

Voles can recognize and distinguish the odors of different predators and take appropriate action. For example, bank voles have a variety of antipredator responses to common weasels and stoats, but fewer reactions to foxes or polecats (Jgdrzejwski et al. 1993). This difference must surely be because in some habitats bank voles contribute more than half the diet of common weasels and stoats (Pekkarinen & Heikkila 1997), but less than 10% of the diet of foxes and polecats (Jgdrzejwski et al. 1993). A vole is safe from a fox in a narrow tunnel, and in the enclosure experiments reported by Jgdrzejwski et al., voles fled into tubes simulating underground burrows when presented with the odor of a fox. But a weasel can follow a vole into a tunnel, so voles presented with the odor of a weasel avoided the tubes and reduced their overall activity for as long as a day or more (Jgdrzejwski et al. 1993; Bolbroe et al. 2000). These antipredator reactions certainly seem to be innate and of long standing, since Orkney voles react to the odor of foxes even though these voles have lived in isolation from foxes since Neolithic times (Calder & Gorman 1991).

On the other hand, although avoiding a weasel is a clear benefit to a vole, a flight reaction that drives a vole into areas that it does not know well may constitute an even greater danger than does a nearby weasel. In addition, prolonged reduction in activity also has a potentially serious cost, in that it must reduce foraging rate and food intake. Over the long term, natural selection favors a compromise between different kinds of risk. Borowski (2000) showed that weasel odor affects the behavior of voles only over short distances and for brief periods, and does not cause a vole to leave its normal home range.

If voles react to the mere odor of a weasel and to its actual presence in similar ways, the impact of weasels on the population dynamics of voles might not be confined to killing those that they can catch. Weasels might also have effects on voles they do not catch, for example, by suppressing their reproductive activity. This hypothesis has had a good run lately, but the jury is still out.

Laboratory experiments indicated that female voles placed in close proximity to a weasel or its odor could slow their estrous cycles, reduce pregnancy rates, increase their aggression toward males when approached even when in estrous, and slow their growth (Ronkainen & Ylonen 1994; Ylonen & Ronkainen 1994; Koskela et al. 1996). Population models suggest that reproductive delays could benefit females in fluctuating populations (Ylonen 1994; Kaitala et al. 1997). But reproductive delays have not been observed by all researchers (Norrdahl & Korpimaki 2000a) nor in all vole species, and the experimental designs of the published studies have been severely criticized (Hansson 1995; Lambin et al. 1995). More realistic enclosure experiments have failed to support the reproductive suppression hypothesis (Wolff & Davis 1997; Mappes et al. 1998).

We do not, however, conclude that weasels have no effect on the reproductive output of their prey. On the contrary, we can see two possible ways in which they might: (1) When food is scarce for voles, for example, during a population decrease, the presence of a resident weasel may cause some voles to delay breeding, because if they move about less to avoid meeting a weasel, they will also reduce their chances of finding a mate, or enough food to support a pregnancy (Korpimaki et al. 1994; Norrdahl & Korpimaki 1995a); (2) if weasels preferred to kill large female voles, those capable of reproduction, disproportionately to their numbers (Klemola et al. 1997; Norrdahl & Korpimaki 1998), that would also decrease the reproductive output of a vole population, yet Y-maze experiments showed that weasels had no clear olfactory preference for any particular category of voles (Ylonen et al. 2003).

The reproduction suppression hypothesis is not quite dead yet, since the hunting behavior of wild weasels is only partially observable in captivity, but we suggest that it is usually a small effect compared with that of direct predation. Death in a weasel's jaws is surely a less subtle but far more effective end to the reproductive prospects of any vole.

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