pers. obs.) then selection should favor the early acquisition
of behaviors that would help young survive a predator en-
counter. Yet newly emergent ground squirrels do not reli-
ably respond to alarm calls, and when they do they tend to
remain in place above ground instead of running to safety.
Juveniles also do not post, which would allow them to lo-
cate the predator visually and monitor its movements (e.g.,
Mateo 1996a). In contrast, competent, adultlike defensive
behavior is present in garter snakes (Thamnophisspp.) at
birth, and responses change very little during early life (Her-
zog and Burghardt 1986; see also Magurran 1990; Cu-
rio 1993). Why, then, do juvenile S. beldinginot emerge
with these skills, which would help them to both detect
and escape from predators at a time when they are most
vulnerable?
The combined needs to develop in the relative safety of
the natal burrow and to emerge above ground and begin
foraging constrain the timing of natal emergence. Over-
winter survival in some ground-dwelling squirrels is depen-
dent upon the acquisition of adequate body fat prior to
hibernation, and more than 60% of juveniles do not sur-
vive their first winter (Barash 1973; Murie and Boag 1984;
Sherman and Morton 1984; pers. obs.). As a result, juve-
niles of hibernating species emerge less physically developed
(i.e., in motor- or sensory-perceptual systems) than juveniles
of nonhibernating species, but demonstrate rapid growth
rates after emergence (Clark 1970; Morton and Tung 1971;
Maxwell and Morton 1975; Koeppl and Hoffmann 1981;
Rickart 1986). For instance, S. beldingijuveniles gain an
average of 2 g /day after birth until they emerge at 27 days
of age at 20% of adult female (mid-season) body weight;
they gain an average of 4 g /day during the 25 days following
natal emergence (Mateo 1995). In comparison, California
ground-squirrel young, which do not hibernate, gain 3 g /day
during their 45-day preemergent period, and emerge at
30% of adult-female weight (usingS. beecheyidata in To-
mich 1962). Thus S. beldingihave a short active season,
emerge at an early age, and as a result may spend less
time with their mothers and littermates, compared with S.
beecheyi. These interspecific differences in developmental
rates as a function of ecological conditions could have sig-
nificant effects on mother-offspring interactions and social
development. Studies of free-living rodents therefore pre-
sent a unique opportunity to examine in detail how the in-
tertwining effects of latitude, elevation, and climate on ac-
tive-season length and pre- and post-weaning growth rates
influence behavioral development.
S. beldingiontogeny entails a compromise between pro-
longed development in the natal burrow prior to emergence
and the need to begin foraging above ground to gain weight
for successful overwintering. As a result, juveniles must at-
tain the motor and perceptual capabilities needed for re-
sponses to complex alarm calls during the postemergent
period, despite their susceptibility to predation. However,
newly emergent juveniles’ limited repertoires, prior to gain-
ing this competence, may be sufficient for them to reduce
their risk of predation, particularly if they are still near the
natal burrow and if the mother is nearby to ward off pred-
ators (Mateo 1996a). Newly emergent juveniles typically
freeze in response to alarm calls rather than respond like
adults. This leaves them vulnerable to predators, but freez-
ing may actually increase their chances of survival. A juve-
nile that seeks refuge in a burrow is safe from visual detec-
tion by a predator, yet a juvenile that remains above ground
may learn to discriminate between stimuli faster by observ-
ing the responses of others (while eliminating movement
cues; see Mateo and Holmes 1997). For newly emergent ju-
veniles then, there is a trade-off between escape responses
and information gathering (fig. 17.3). Further, if the likeli-
hood of an individual actually encountering a predator is
small, then the benefits of remaining above ground and ob-
servant can outweigh the costs of prolonged exposure.
Therefore, selection has favored early natal emergence
by Belding’s ground squirrels over prolonged preemergent
maturation, with the costs of limited motor capabilities off-
set by the benefits of observational learning and rapid ac-
quisition of discriminating responses. Consequently, the de-
velopment of juvenile S. beldingiantipredator repertoires,
particularly the patterns of responses that require motor co-
ordination, may reflect neural and physical development,
whereas behavioral discrimination among calls is influenced
by experience with the auditory stimuli and observations of
conspecifics (Mateo 1996a, 1996b; Mateo and Holmes
1997). In contrast, juvenile S. beecheyihave a longer pe-
riod of preemergent development (see earlier comments),
and perhaps as a result they show well-formed, adultlike,
behavioral responses to rattlesnakes despite not having ac-
quired adult levels of venom resistance (Coss 1991a; see
also Owings and Coss, chap. 26, this volume). These find-
ings illustrate the importance of viewing juvenile behaviors
as a series of adapted phenotypes appropriate for each stage
of development, rather than impoverished approximations
of adult behavior (Williams 1966; Galef 1981b; Owings
and Loughry 1985; Alberts 1987).Other Issues in the Study of
Behavioral DevelopmentLength of parental dependence
There is much variation across vertebrates in the degree
to which parents protect their young from predators. This
variation is, in part, correlated with the length of timeOntogeny of Adaptive Behaviors 201