tively large populations of prey and predators and to display
the oscillatory dynamics of classical predator-prey models.
Fear-driven systems are likely to see relatively smaller pop-
ulation sizes of predators and to display more stable popu-
lation dynamics. In m-driven systems predators have strong
negative direct effects on themselves through the fear re-
sponses they induce in their prey (Brown et al. 1999).
We suggest that voles and their predators (particularly
weasels) represent primarily N-driven systems, whereas
most desert rodents represent m-driven systems. Produc-
tivity and diet may explain these differences. Most voles,
especially Microtus,feed from a food source that is of low
quality and occurs at high productivity, in contrast to most
desert rodents, for which the opposite is true. Voles exhibit
less long-term caching behavior, except for the root vole
(Microtus oeconomus)andClethrionomysspecies. The lack
of food caching requires voles in general to feed frequently,
even in the face of danger, and to “store” food in the
form of fecundity. Granivorous desert rodents enjoy a high-
quality, highly cacheable food. This food and foraging be-
havior allows desert rodents to forgo both foraging and
reproduction during times or places of high predation risk.
While denying itself immediate offspring, the granivorous
desert rodent also denies the predator its lunch. Obviously,
voles can and do respond to predation risk, and obviously
desert rodents suffer predation, but on the continuum be-
tween totally N-driven and totally m-driven systems it is
likely that boreal voles are more N-driven and less m-driven
than are most desert rodents.
Fear from Multiple Predators:
Birds, Mammals, and Snakes
The expression “[the] fangs of the snakes are driving gerbils
into the talons of the owls” (Kotler et al. 1992, p. 155) de-
scribes a trade-off in the decision-making process of rodents
that are faced with risks from multiple predator species
(Lima 1992). Predator facilitation(Charnov et al. 1976) is
the term used for tactics that reduce mortality from one
type of predator while increasing the chances of falling prey
to another predator species. This pattern as described for
desert habitats is true for more covered habitats as well
(Korpimäki et al. 1996). Terrestrial predators such as mam-
mals and snakes often use ambush tactics in hunting. Hab-
itats with cover offer the predator concealment while it
awaits the approach of a potential prey. In contrast, com-
plex vegetation cover reduces the effectiveness and lethal-
ity of avian predators such as owls and hawks. Thus, ro-
dents face multiple fears and potentially conflicting hazards
when choosing activity patterns among spatial (shrub ver-
sus open) and /or temporal habitats (day versus night, moon
phase, etc.).
An important alternative activity for rodents (or any
prey) is to remain inactive in a safe place or burrow. In op-
timal foraging models, remaining safely inactive becomes
attractive when all foraging opportunities have been de-
pleted to the point that the harvest rate, H,from foraging
no longer exceeds the metabolic cost, C,predation cost, P,
and missed opportunity cost of foraging, MOC;i.e., indi-
viduals cease foraging activity when HCPMOC
(Brown 1988, 1992). Here the missed opportunity cost is
the negative of the sum of the resting metabolic cost and the
cost of predation while inactive in a burrow or safe retreat.
Presumably, the metabolic and predation costs of resting
are lower than those when foraging. If safety in the rodents’
burrow is relatively low due to predators, such as snakes
and weasels, that are able to hunt in the burrows of rodents
(L. Oksanen and Lundberg 1995; Ylönen et al. 2003), then
there are fewer advantages for decreasing foraging activity
and remaining inactive in one’s burrow. This may be an-
other driver for the different activity patterns seen in desert
rodents and voles. Desert rodents may experience higher
costs of predation while foraging than do voles, and they
may experience lower costs of predation while remaining
inactive in their burrow. The difference in degree of safety
in and out of the burrow may be less for voles than for des-
ert rodents.
Biologists have studied antipredatory responses of ro-
dents by offering them choices of habitats that differ in risk.
As expected, under equal feeding opportunities rodents
bias their activity toward safer habitats (Brown et al. 1992;
Kotler and Blaustein 1995; Jacob and Brown 2000). In
the case of predator facilitation from terrestrial preda-
tors and avian predators, rodents bias their foraging activ-
ity toward the microhabitat with cover in response to owls
(Brown et al. 1988; Kotler et al. 1991; Brown et al. 1992;
Kotler and Blaustein 1995; Kotler 1984) and toward the
open microhabitat in response to snakes (Brown 1989;
Bouskila 1995) or terrestrial mammals (Korpimäki et al.
1996). Lima (1992) suggests that the responses of prey to
the presence of multiple predators should differ from sit-
uations with just one predator species. The addition of
the second predator into the system may actually decrease
prey vigilance, because the prey aim to minimize their time
exposed to predators by decreasing the time they spend
foraging.
Experiments with simultaneous risks from two predator
species are more difficult to design and control than those
with just one predator species. In desert rodents, Kotler
and colleagues have manipulated owl and snake predation,
illumination, and habitat properties in large aviaries (e.g.,Fear and the Foraging, Breeding, and Sociality of Rodents 335