contexts has uncovered significant structural differences
(Leger et al. 1980; Owings and Leger 1980). Perhaps use of
these calls in both contexts has favored structural differen-
tiation to minimize the impact of each type of use on the
functionality of the other system. If squirrels distinguish so-
cial and antipredator variants, then dilution of antipredator
function may not be a problem, even if conspecifics are pri-
mary targets. However, Tamura’s (1995) research on For-
mosan squirrels suggests that this species does not distin-
guish calls used in the two contexts. Playback studies have
not yet ascertained whether these differences have commu-
nicative significance for California ground squirrels.
A second under-explored feature of such calling is that
many sciurids and other species also call tonically (as in
Schleidt 1973), that is, repetitively throughout an encounter
with a predator or conspecific and even into the aftermath
of encounters (Betts 1976; Smith et al. 1977; Boellstorff
et al. 1994; Warkentin et al. 2001). These rhythmically re-
peated calling patterns regulate the behavior of conspecifics
or heterospecifics by fostering a sustained state in targets —
for example, of vigilance or immobility, rather than by elic-
iting a discrete response as initial calls often do (Owings
et al. 1986; Loughry and McDonough 1988). Tonic anti-
predator calling may be functionally distinct; for example,
working selfishly when initial calls function nepotistically
even though initial callers and tonic callers are typically the
same individuals (Owings et al. 1986). More work needs to
be dedicated to exploring what temporally extended regu-
latory problems callers “solve” with these temporally ex-
tended patterns of vocal communication. Tonic antipreda-
tor patterns appear in part to be adaptations to predators
that pose a more temporally extended threat — for example,
because they lie in ambush for extended periods (Hanson
2003).
Shared components at the level
of animal-environment integration
The stress-response system
Even though social and antipredator systems are typically
functionally distinct, they are linked causally, because both
conspecifics and predators can be sources of stress. Male
California ground squirrels, for example, fight intensely
with other males during the approximately 2-week breed-
ing season, resulting in extensive wounding (Owings et al.
1979; Boellstorff et al. 1994). Similarly, California ground
squirrel females expose themselves to substantial stress dur-
ing their single day per year of estrus, soliciting courtship
from multiple males, intensely resisting all males after they
have mounted, but copulating with many of them (Boell-
storff et al. 1994; unpublished observations). Later in the
reproductive season, females also experience stress from
predators; for example, as rattlesnakes move in to prey
on the developing young (our earlier scenario; Hennessy
and Owings 1988). Mammalian and avian predators also
endanger both pup and adult California ground squir-
rels, inducing stress not only through actual encounters but
also indirectly through the antipredator vocalizations these
predators elicit (Leger and Owings 1978; Owings and Vir-
ginia 1978; Leger et al. 1979; Owings and Leger 1980). Fi-
nally, social and predatory threats can at times be generated
by the same individual; some female California ground
squirrels and some members of other sciurid species are in-
fanticidal, and may kill multiple offspring of other females
(Sherman 1981b; Hoogland 1985; Trulio et al. 1986; Lacey
1991; Lacey 1992; Trulio 1996; Ebensperger and Blum-
stein, chap. 23 this volume).
Rodents typically cope with such threats of injury or
other forms of harm by making physiological and behav-
ioral adjustments that can increase their ability to escape
or resist a threat (Koolhaas et al. 1999). These adjustments
are supported by several different physiological systems, in-
cluding the hypothalamic-pituitary-adrenal (HPA) stress-
response system (Sapolsky 1992; Francis and Meaney 1999;
Perrot-Sinal et al. 1999), and neurotransmitter/neuromod-
ulatory systems based on the morphine-like peptides (en-
dorphins) and the benzodiazepine-GABA neurotransmitter
system (Kavaliers 1988; Edwards et al. 1990).
Activation of the HPA system contributes to many phys-
iological and behavioral adjustments that facilitate coping
with emergencies. Releasing glucose stores, inhibiting glu-
cose storage, and increasing breathing rate, heart rate, and
blood pressure all fuel physical efforts to escape or resist
a threat. Blocking inflammation maintains joint mobility
even when the joint has been injured, and so facilitates per-
formance of the actions of offense and defense (Sapolsky
1992). Boosting dermal immune function can enhance re-
sistance to pathogens that may invade cuts or punctures
(Dhabhar and McEwen 1999). The effects of psychological
changes complement those of these physiological adjust-
ments. Increasing vigilance enhances the probability that
sources of danger will be detected. Redirection of the focus
of learning and memory systems to emotion-laden events
and places facilitates learning that provides emotional labels
for environmental situations; this in turn enhances antici-
pation of and preparation for danger (Francis and Meaney
1999).
Stress-induced analgesia is mediated by at least two neu-
ral systems: an endorphin-based neurotransmitter and neu-
romodulator system (Lester and Fanselow 1985; Kavaliers
1988; Hendrie 1991) and a benzodiazepine-GABA neuro-
transmitter system (Edwards et al. 1990). These systems
appear to work in complementary time frames when acti-
vated by perception of a predator such as a weasel (Kava-308 Chapter Twenty-Six