Kotler et al. 1992, 2001). In boreal voles, large-scale field
or aviary studies with multiple predator species have been
lacking. A study with combined avian and weasel predation
risk (Korpimäki et al. 1996) was conducted in small labo-
ratory arenas. However, J. Eccard and colleagues (2001)
managed to document significant increases in risk taking
in the foraging behavior of bank voles in an enclosure ex-
periment where voles were exposed to freely hunting wea-
sels and long-eared owls simultaneously. Despite the risk
posed by weasels hunting in covered microhabitats, voles
increased their use of this microhabitat because of the even
stronger threat posed by owls in more open microhabitats.
Interestingly, the presence of owls forced the least wea-
sels to be more cautious when moving through open areas,
and the presence of owls may have reduced the lethality of
weasels to the voles. To the owls, the presence of weasels
may have provided a prey in itself and made the voles eas-
ier to catch. To the weasels, the owls may have reduced their
hunting efficiency, because the weasels now had a height-
ened foraging cost of predation.
Breeding and Predation Risk
Applying a Russian proverb to female mating strategies,
L. Oksanen and Lunberg (1995, p.46) point out that a fe-
male “cannot be a little bit of pregnant.” A female faces
the trade-off between reproduction and survivorship. The
breeding suppression hypothesis (Ylönen 1989, 1994b; Ylö-
nen and Ronkainen 1994) predicts that females should favor
survivorship over reproduction during the declining phase
of a vole cycle and fecundity over survivorship during the
increase phase. The hypothesis assumes that female repro-
ductive activities increase the risk of predation, especially
when vole-specialist predators such as small weasels are
abundant (sensuCushing 1985). In northern cyclic vole
populations where predation risk also fluctuates cyclically,
females that delay breeding during the high-risk phase en-
hance their fitness by increasing their survivorship and by
depositing their offspring into the low-risk phase of the cycle
(see L. Oksanen and Lundberg 1995).
Initial testing of breeding suppression hypothesis in the
laboratory reported obvious effects of simulated weasel
predation risk on the reproduction and reproductive be-
havior of voles (e.g., Heikkilä et al. 1993; Ylönen and
Ronkainen 1994; Ronkainen and Ylönen 1994; Koskela
and Ylönen 1995; Koskela et al. 1995). When high weasel
abundance foiled an otherwise optimal breeding season, re-
production by voles in the field was lower than predicted
(Korpimäki et al. 1994). However, all field attempts to use
mustelid scent to simulate increased predation risk have
failed to produce changes in female reproductive behavior
consistent with the breeding suppression hypothesis (see
Parsons and Bondrup-Nielsen 1996; Wolff and Davis-Born
1997; Ylönen 2001, for review). Despite obvious behav-
ioral responses to predation risk, trading off reproduction
for future survival does not seem to maximize individual fe-
male reproductive success. For voles that are short-lived
and cannot store food for long periods and that must feed
frequently, it may be maladaptive to forgo breeding dur-
ing the short breeding seasons offered by higher latitudes.
In fact, voles have adaptations like postpartum estrus and
other physiological adaptations for avoiding even short de-
lays in subsequent litters. Maximizing breeding effort and
producing as many young as possible and as quickly as pos-
sible is probably the best strategy for maximizing lifetime
reproductive success (Kokko and Ranta 1996).
The field studies previously mentioned simulated in-
creased predation risk during the best of breeding cir-
cumstances: namely, under conditions of moderate vole
densities and abundant food resources. The breeding sup-
pression hypothesis may apply to voles under less favorable
feeding conditions — for instance, very early in the breeding
season or for late breeders. During these less favorable feed-
ing conditions, reductions in activity caused by increased
risk of predation may place female voles below a threshold
breeding condition. Theoretically this strategy would re-
semble the “waiter” strategy and represent a compromise
between the strict reproducers or strict survivors of L. Ok-
sanen and Lundberg (1995). Carlsen et al. (1999) examined
the effects of predator scent on the body mass and survivor-
ship of field voles over winter. They observed the same trend
that Dickmann (1992) noted for house mice and Norrdahl
and Korpimäki (1998) for field voles. Under low predation
risk, survivors were heavier, either because predation that
targeted heavier individuals was lacking or because voles
fed more under low predation risk.
A study of grey-sided voles (Clethrionomys rufocanus)
in subalpine tundra in northern Norway supported the pre-
dictions of the breeding suppression hypothesis even dur-
ing a summer breeding season (Fuelling and Halle 2004).
A significantly higher proportion of reproductively inactive
adult females occurred on plots treated with weasel scent as
compared to control plots. Control plots saw a higher num-
ber of juveniles recruited into the adult populations. One
interpretation of these results is that breeding suppres-
sion may occur as a consequence of energy limitations
in harsh environments or under less favorable conditions
at the boundaries of the breeding season (Norrdahl and
Korpimäki 2000). Breeding suppression by voles is prob-
ably not an evolved antipredator strategy. Evolved breeding
suppression as outlined in the breeding suppression hy-336 Chapter Twenty-Eight