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Development of bite strength and feeding behaviour in juvenile

spotted hyenas (Crocuta crocuta)


Wendy J. Binder and Blaire Van Valkenburgh
Organismic Biology, Ecology and Evolution, University of California, Los Angeles, 621 Circle Drive South, Los Angeles, CA 90095-1606, U.S.A.
(Accepted 26 October 1999)
Abstract
Bite strength is of great importance to carnivores, as their jaws must produce forces of sufcient magnitude
to kill and consume their prey. Spotted hyenas, well known for crushing and consuming bones, were
studied to determine how tooth and jaw growth affect bite strength and feeding behaviour. Nine captive
individuals, aged 6 months to 2 years of age, were sampled as they grew. At 8- to12-week intervals,
morphological measurements that estimated jaw muscle mass, tooth size and skull size were taken. Using a
force transducer, bite force was measured directly for these juveniles as well as other captive individuals of
different ages. In addition, feeding behaviour and performance were quantied periodically by bone tests
in which individuals were offered a sheep femur for 15 min. Behaviour and performance were expected to
change with the shift from juvenile to adult dentition. Results were not entirely as expected. Morphological
measurements of growth reached a plateau at about 20 months, whereas bite strength increased in a linear
fashion up to 5 years of age. A fundamental change in tooth use during bone cracking followed the
replacement of deciduous teeth with permanent teeth; the primary area of tooth use moved from anterior
to rearmost premolars, increasing the mechanical advantage of the jaw adductors. The timing of this shift
seemed to be a function of a decrease in gape limitation as a result of growth as well as caudal movement
of the premolars. Our data demonstrated that juvenile hyenas had not achieved adult feeding performance
levels at 12 months of age, when they are typically weaned in the wild. This suggests that recently weaned
cubs may be at an increased risk of starvation and that selection might favour later weaning times.
Key words: hyena, bite strength, skull development, feeding behaviour, Crocuta crocuta
INTRODUCTION
Performance has been dened by Wainwright (1994) as
the ability of an organism to accomplish specic beha-
viours and ecologically relevant tasks. An individual's
morphology, which changes with growth, can determine
the limits of its performance, and can inuence its
ability to thrive in its environment. As carnivores make
their living by killing and consuming prey with their
teeth and jaws, and as young carnivores are often
subordinate to but have greater urgency to feed than
adults, the development and performance of the jaws is
a subject of great interest.
The spotted hyena Crocuta crocuta is a species in
which feeding performance is especially likely to be
under strong selection. Spotted hyenas are social animals
that hunt and kill like members of the Canidae, with
cheek teeth and jaw characteristics that more closely
resemble those of the Felidae (Ewer, 1973; Biknevicius &
Ruff, 1992; Gittleman & Van Valkenburgh, 1997).
However, spotted hyenas are distinguished by their
exceptionally enlarged premolars, robust skulls and
teeth, all of which reect their habit of regularly con-
suming large bones (Werdelin, 1989; Biknevicius & Ruff,
1992; Rensberger, 1995). Feeding can be a highly compet-
itive activity, especially when hyenas are numerous and
food is scarce (e.g. the dry season in eastern Africa)
(Kruuk, 1972; Tilson & Hamilton, 1984; Holekamp &
Smale, 1990). During these times, the group will nish a
carcass rapidly and often individuals must quickly use
whatever portion they can procure, be it pliant, tough or
brittle. Not all individuals have equal access to both
meat and bone. The highest ranking individuals have
rst access to kills, followed by lower ranking and
smaller individuals (Tilson & Hamilton, 1984; Henschel
& Skinner, 1987; Frank, Glickman & Zabel, 1989). The
jaws of juveniles, which are not completely developed,
produce smaller bite forces than those of adults. Selec-
tive pressure on cubs (especially on sub-dominant cubs)
for rapid feeding, and for any specializations of the teeth
and jaws that enable them to feed more efciently, is
expected to be signicant. For example, adaptations that
J. Zool., Lond. (2000) 252, 273283 #2000 The Zoological Society of London Printed in the United Kingdom
result in an earlier acquisition of adult levels of bite
strength might be favoured. Thus the development of the
skull and teeth, and how they affect both access to food
and the ability to consume it completely and rapidly
probably play a large part in survival.
Spotted hyenas are born into matrilineal, hierarchical
clans of up to 80 individuals (Kruuk, 1972). Although
spotted hyena cubs are born precocial relative to most
ssiped carnivorans (members of the Carnivora), they
are fed almost exclusively on milk for the rst 58
months of life (Van Jaarsveld, Skinner & Lindeque,
1988; Holekamp & Smale, 1990), and their weaning
time seems delayed relative to other carnivorans
(Gittleman, 1986). The young join the adults in feeding
on meat regularly at about 8 months, and eat meat
exclusively by about the age of 1218 months (Kruuk,
1972; Ewer, 1973; Mills, 1990). Deciduous cheek teeth
begin to erupt at 6 months, with adult teeth completely
erupted between 12 and 14 months, the typical age
of weaning (Kruuk, 1972; L. Frank, pers. comm.).
Mothers rarely bring food to the den, nor do they
regurgitate food to their cubs, so once the cubs eat meat
they must acquire it from common prey items by
themselves (Frank, 1986; Holekamp & Smale, 1990;
Mills, 1990). Their ability to process a carcass effectively
seems to be dependent on the rapid development of
adult levels of bite strength.
Although bite force is expected to increase with age,
there are no data concerning the rate and trajectory of
the increase, or how it might relate to weaning age.
Moreover, little is known about how the development
of bite strength is affected by the change from juvenile
(deciduous) to adult (permanent) dentition, or the inu-
ence of both of these on feeding behaviour. It is possible
that the transition between juvenile and adult dentition
is accompanied by reductions in feeding efciency,
especially when deciduous teeth are delicate or missing
as the adult teeth erupt. This might be manifested by a
transient drop in bite strength and alterations in feeding
behaviour.
In this paper we address several questions concerning
growth, bite strength and feeding performance in the
spotted hyena. First, how does skull morphology and
tooth size change with age? Second, how does bite
strength change with age? Third, how does feeding
behaviour change with age, and how does it relate to
changes in morphology and bite strength? Lastly, what
are the implications of our results for wild spotted
hyenas?
MATERIALS AND METHODS
Data from living spotted hyenas in this study come
from a colony of captive individuals housed at the
Field Station for Biological Research at the University
of California at Berkeley. Approximately 40 spotted
hyenas currently reside there, including the initial group
of 20 wild-captured individuals from Kenya and
their progeny. Individuals of various ages are present,
including several cohorts of similarly aged individuals,
some of whom are siblings, raised together. Data and
results are presented from 9 adults (4 males, 5 females)
and 3 mixed-sex cohorts of young, including a pair of
siblings, a group of 5 (including 2 sib-pairs and a fth
similarly aged juvenile), and a third sibling pair. Indivi-
duals were followed for 3 years, and data were collected
at 8- to 12-week intervals. During the study, sampled
individuals ranged in age from 6 months to 40 months,
depending upon their ages at the time the study began
(or time of birth during data collection). Weaning time
in the colony was substantially earlier than that in the
wild, occurring on average at 6 months, as opposed to
an average of c. 12 months in the Masai Mara, Kenya
(Holekamp, Smale & Szykman, 1996). Because nearly
all of the data presented here are from weaned cubs, we
could not observe the effect of weaning on feeding
behaviour. Standard statistical tests were run, including
linear regressions, Spearman correlations, and Mann
Whitney U-tests.
Morphological measurements
Tooth row length and 7 measurements of skull shape
and size were taken on anaesthetized juvenile hyenas,
approximately every 3 months, up to 3 years of age
(Table 1). Measurements were chosen to reect jaw
muscle development as well as overall size. For example,
maximal skull width across the zygomatic arches should
reect jaw adductor mass, and distances between the
jaw joint and various teeth can be used as estimates of
out-lever moment arm length for a bite at a given tooth
position (cf. Turnbull, 1970). Unfortunately, in-lever
measures for the jaw adductors could not be estimated
from external measures on living specimens. Conse-
quently, it was not possible to track changes in jaw
muscle mechanical advantage with age. However, this
was done in a separate study of museum material
(Binder, 1998). Concurrent with skull measurements,
mesiodistal lengths at the gumline of all visibly erupted
teeth on the left side were taken with digital callipers
(Table 1).
Bite force measurement
Bite force was measured with a force transducer similar
to those used by previous workers (e.g. DeChow &
Carlson, 1983; Thomasen, Russell & Morgen, 1990;
Oyen & Tsay, 1991). The transducer resembles a large
tuning fork made of 2 parallel aluminium beams, with 2
strain gauges in a full Wheatstone bridge conguration
glued to the inner surface of each beam (Fig. 1). We
used 2 transducers: a `juvenile' device with longer arms,
which is more sensitive to bending forces and able to
transmit signals for less forceful bites, and an `adult'
device with shorter arms that transmits signals for a
larger range and magnitude of bite forces. Each biting
fork has a rubber-covered biting area (of c. 1 cm
2
) at the
W. 1. BiNnr :Nn B. V:N V:ixrNnicn 274
distal end of each beam. The biting area was covered
with rubber and duct tape to protect the teeth of the
animals. When a hyena bit the distal end of the fork, the
arms were bent towards one another and this compres-
sive load was registered by the strain gauges as voltage
changes. Voltage data were recorded in real time using a
MacLab data recorder, converted from analogue to
digital format and downloaded to a laptop computer.
The resulting data were then converted from voltage
into newtons of force based on a prior calibration of the
devices with an Instron materials testing machine, a
machine capable of applying known compressive or
tensile loads to an object.
Bite forces were recorded for non-anaesthetized indi-
viduals who voluntarily bit the transducer device when
it was introduced into their enclosure through openings
in the surrounding fence. Individuals that chose to bite
the device were typically actively engaged in their
efforts. They usually attempted to wrest the device from
the data collector and pull it into their enclosure, but
were prevented from doing so because the handle of the
device did not t through the fence. Maximum bite
force data were collected for each of 2 teeth areas,
consisting of the most posterior premolars and the most
anterior incisors, as chosen by the individual hyena.
Both force transducers were used, but the juvenile
device was employed primarily for younger juveniles up
to c. 16 months of age, and the adult device was used
from c. 12 months to all ages of adulthood. During the
period of overlap in age (1216 months), both devices
were used, which conrmed that the devices remained
cross-calibrated. At no time did either device reach a
maximum (at-line) voltage indicating that the beams
were touching at the distal tips.
Feeding behaviour and performance
Feeding performance was assessed by bone cracking
behaviour in a series of `bone crunching tests'. Bone
crunching tests consisted of sessions during which a
food-deprived (for a minimum of 24 h), isolated hyena
was given a single, deeshed sheep femur of known
weight (200380 g), and then closely observed for 15
min. All the data presented here were collected by 1
observer. The observer collected several categories of
data, listed in Table 2.
Although additional data such as forelimb use in food
manipulation were collected, the feeding behaviour data
presented here are limited to those variables concerned
with tooth use. Tooth use was divided into use of
incisors, front premolars and rear premolars. Based
upon examination of skulls, front premolars (lower dp2,
dp3 and P2, P3) were considered to be teeth directly
under and/or anterior (and ventral) to the eye, and rear
premolars (lower dp4 and P4) were considered to be
posterior (and ventral) to the eye. This spatial relation-
ship between eyes and teeth was true for hyenas of all
ages.
Data were collected simultaneously by holding down
275 Bite strength and feeding in spotted hyenas
Table 1. Measurements taken from anaesthetized, growing hyenas. All measurements were taken from the left side; tooth
measurements taken at the gumline. Length measurements taken with measuring tape, large callipers and small callipers,
depending upon size
Measurement Denition
Weight (kg)
Body length (mm) From nose to base of tail
Head circumference (mm) Around head at widest point of zygomatic arches
Head width (mm) At widest point of zygomatic arches
Head length (mm) Tip of nose to caudal tip of nuchal crest
Ear to canine (mm) Most rostral part of external ear to rostral side of lower canine
Ear to third premolar (mm) Most rostral part of external ear to caudal side of lower third premolar
Toothrow (mm) Distal end of most posterior upper tooth to between upper rst incisors
Canine height (mm) Crown height measured from gumline to canine tip
Tooth lengths (mm) Mesio-distal lengths of each tooth at gumline
Fig. 1. Bite force device, showing location of strain gauges (A), and where bite force is applied (B).
keys on a recorder, and the percentage of total time
spent at each activity was collected at the end. If an
animal nished its bone before the end of 15 min, the
percentages were calculated for the time used to nish
the bone. Because several behaviours were recorded
simultaneously (e.g. paw use and tooth use), percentages
of time spent in any group of activities do not necessarily
add to 100%.
All bones were weighed before the tests, and re-
weighed after the test when they were recoverable.
Feeding performance was estimated in 2 ways: rst, the
total weight of bone consumed in the 15-min test and
second, the time taken to nish a bone. The rst
measure was available when the bone was entirely
consumed, as well as for when it was not entirely
consumed and we could recover the uneaten portion.
The second measure of feeding performance was only
possible when the bone was completely consumed.
RESULTS
Morphology
Not unexpectedly, adults had larger skulls and presum-
ably larger jaw muscles than juveniles. All cranial
measures showed an initial exponential growth trajec-
tory that reached an asymptote at c. 20 months of age
(Fig. 2a). This included maximum skull width across the
zygomatic arches, our indicator of jaw adductor muscle
mass, demonstrating that adults surpassed juveniles for
this determinant of relative bite force. For comparative
purposes, linear regression analyses were performed for
each measurement (log
10
transformed) against age (also
log
10
transformed) in days. All measures of somatic
growth were very similar in having highly signicant
Spearman correlation P-values, and r
2
values between
0.89 and 0.93 (Table 2).
The relationship between tooth-length measures
(taken mesiodistally at the gum-line) and age displayed
a different pattern of change than cranial growth
measures. It proceeded in two distinct steps, the rst
being the complete eruption of deciduous teeth, fol-
lowed by a rapid transition to the adult teeth (Fig. 2b).
For all teeth except incisors, the deciduous dentition
erupted after birth. Spotted hyenas are remarkable
among mammals in being born with a complete set of
upper and lower incisors (Frank, Glickman & Licht,
1991). Deciduous teeth are replaced, starting with upper
and lower incisors at about 6 months, with full eruption
W. 1. BiNnr :Nn B. V:N V:ixrNnicn 276
Table 2. Regression lines, r
2
values, Spearman rho values and P-values of several measures of somatic growth against
log-transformed age
Equation of regression line of log
10
body
Body measure measure and log
10
age
a
r
2
Spearman rho P
Third premolar length (mm) Y=1.686 +0.218X 0.895 0.958 <0.0001
Canine length (mm) Y=1.461 +0.231X 0.919 0.977 <0.0001
Ear to third premolar (mm) Y=1.949 +0.25X 0.914 0.958 <0.0001
Ear to canine (mm) Y=2.041 +0.237X 0.924 0.965 <0.0001
Head circumference (mm) Y=2.452 +0.213X 0.908 0.965 <0.0001
Weight (kg) Y=0.689 +0.806X 0.908 0.960 <0.0001
Head length (mm) Y=2.14 + 0.235X 0.926 0.975 <0.0001
Head width (mm) Y=1.909 +0.239X 0.922 0.975 <0.0001
a
Equations are of the form Y=b +mX, with Y=log
10
(body measure), X=log
10
(age).
(a)
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Age (months)
(b)
Fig. 2. (a) Head width and head length measurements with
age, showing an initial exponential growth period, followed by
slower growth, and asymptotes at c. 20 months of age. Open
circles, head length; crosses, head width. (b) Mesiodistal widths
of the upper third incisor and the lower second premolar from
a group of growing hyenas Crocuta crocuta, showing two
peaks in width as each set of teeth erupt. Open circles, lower
second premolar length; crosses, upper third incisor length.
of the permanent dentition between 12 and 14 months
of age.
Bite force
The results included here are maximum bite forces per
trial for those trials when individuals demonstrated an
active interest and effort in biting. A time series of
samples was taken from several hyenas, tested from
about 6 months (when they would rst bite the device)
to the age reached when data collection ended (2448
months of age). Other individuals were tested only as
juveniles or only as adults. Included here are sequential
data from growing individuals as well as single or
multiple data points from several individuals.
Bite force increased gradually but signicantly with
age, up to c. 6080 months, as evidenced in graphs
based on multiple individuals (Fig. 3a) as well as those
that track single individuals (Fig. 3b). This positive
correlation between age and bite force remained consis-
tent, even when the data were split into various subsets
by: (1) sex; (2) age, excluding all individuals older than
48 months (in order to demonstrate that the trend was
not driven by few extraneously large points); and (3) the
two tooth areas used in biting.
Notably, bite force continued to improve with age in
adults, well after the permanent dentition (1214
months) was in and the skull size seemed to have
nished growing (20 months). Bite strength increased
fairly rapidly up through 5 years (60 months) of age,
and seemed to plateau between 5 and 6.5 years (80
months) (Fig. 3a).
Feeding behaviour
Tooth use in feeding is expressed as the percentage of
time spent using the three different tooth areas (incisors,
anterior premolars or rear premolars) during a 15-min
bone test. The data revealed considerable scatter, espe-
cially for younger individuals (Fig. 4a). Nevertheless,
there were some signicant trends. Between the ages of
4 and 30 months, time spent chewing with incisors
declined slightly but signicantly (r
2
=0.15, Spearman
rho =0.073, P=0.0001) (Fig. 4a). A similar but stronger
trend was seen in usage of front premolars (r
2
=0.501,
Spearman rho =70.696, P=<0.0001) (Fig. 4a). Notably
the variance in time spent using premolars (and incisors)
decreased dramatically among older individuals, with
individuals all behaving more similarly after about
18 months of age.
The opposite trend occurred with rear premolar use;
percentage of time spent chewing with the rear premo-
lars increased with age, to a lesser yet still statistically
signicant degree (r
2
=0.137, Spearman rho =70.396,
P<0.0001), but with no decrease in variance. To better
view these changes, the results were grouped into two
age categories: tooth use up to 15 months of age (when
all teeth had erupted, but well before changes in tooth
use had ceased); and tooth use in individuals over
15 months of age, by the three `tooth areas' (Fig. 4b). It
is clear that there was both a reduction in the amount of
time individuals spent using their front teeth, and a
pronounced increase in the amount of time spent using
rear teeth, and each change was signicant.
Feeding performance
Despite the wide scatter in the data, there was a
signicant increase in the amount of bone consumed
with age (Fig. 5a). Although there were always some
individuals that just consumed a small amount, only
older individuals (of at least 17 months of age) con-
sumed most or all of the bone within 15 min.
The second feeding performance measure was that
of time needed to completely consume the bone within
the allotted 15 min (Fig. 5b). The data show more
scatter than in the previous performance measure, but
277 Bite strength and feeding in spotted hyenas
(a)
5000
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0
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0 20 40 60 100 120 140 160 180
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1400
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10 15 20 25 30 35 40 45
Age (months)
(b)
Fig. 3. (a) Maximum measured bite force of living hyenas with
age, including bites at the incisors and premolars. Some points
are from the same animal at different ages. Bite force
=165.952 +12.683 * age; r
2
=0.615, Spearman rho =0.762,
P<0.0001. (b) Maximum measured bite force of living hyenas
with age, showing a data series for two individuals; Nairobi:
bite force =757.134 +32.074 * age; r
2
=0.522, Spearman
rho =0.786, P<0.0065; Nakuru: bite force =7134.791
+33.232 * age; r
2
=0.815, Spearman rho =0.893, P<0.0031.
Open circles, Nakuru (female); crosses, Nairobi (female).
individuals were compared across a much more limited
age span. Notably, none of the nine tested individuals
younger than 17 months nished a bone within 15 min.
Once they began to nish bones, they continued to
improve in average speed of ingestion (Fig. 5b). There
seemed to be a marked jump in maximum speed at
2122 months of age (P<0.05, MannWhitney U-test).
Before this age, not one individual consumed a bone in
<6 min.
DISCUSSION
Skull growth and dental eruption
As expected skull morphology followed an exponential
growth curve, reaching an asymptote at c. 20 months of
age. This was true for all somatic measures of skull
growth, including measures related to relative bite force,
such as zygomatic width and the distance between bite
points and the jaw joint. In the wild, overall body size
seems to increase until about 30 months of age in males,
and 36 months in females (Mills, 1990).
Because the mass of the jaw muscle is reduced in
juveniles relative to adults, they might compensate for
this weakness by enhancing bite force through better
leverage for the primary jaw adductor, the temporalis
muscle. This could be accomplished by positioning the
deciduous carnassials and premolars closer to the jaw
joint (shortening the out-lever) and/or enlarging the
coronoid process of the mandible (lengthening the in-
lever). However, this does not seem to be the case.
Although we could not estimate temporalis muscle in-
lever on the captive hyenas, our measures of out-levers
and those of Biknevicius (1996) reveal that the decid-
uous teeth were positioned farther forward in juveniles
than adults. This may be the result of tooth germ
position; as the tooth germ of the lower molar is
posterior to that of the premolars (deciduous and
adult), it may not be possible to shift the deciduous
W. 1. BiNnr :Nn B. V:N V:ixrNnicn 278
90
80
70
60
50
40
30
20
10
0
0 5 25 30
Age (months)
P
e
r

c
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n
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o
f

t
i
m
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c
h
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w
i
n
g

w
i
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a
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t
e
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t
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T
i
m
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t
o
o
t
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u
s
e

(
%
)
60
50
40
30
20
10
0
Incisors Front
premolars
Rear
premolars
Bone tests up to age 15 months
60
50
40
30
20
10
0
Incisors Front
premolars
Rear
premolars
Bone tests after age 15 months
(a)
(b)
Fig. 4. (a) Percentage of time spent chewing bone in `bone crunching test' using front premolars (open circles) and incisors (solid
circles), showing a decrease in use of both with age. The data presented include points representing an age series in several
individuals (ages span between 12 and 36 months, depending upon the ages of the individual hyenas when data collection began
and ended). Incisor use =27.616 0.501 * age; r
2
=0.147, Spearman rho =70.439, P<0.0001; front premolar use =52.829
1.707 * age; r
2
=0.501, Spearman rho =0.696, P<0.0001. (b) Changes in the percentage of time in which incisors, front
premolars and rear premolars are used in bone tests given up to 15 months of age, compared with bone tests given after
15 months of age; MannWhitney U-test, incisors: U=1133.5, P<0.0001; front premolars: U=444.5, P<0.0001; rear
premolars: U=1127.5, P<0.0001.
(a)
(b)
P
e
r
c
e
n
t
a
g
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o
f
t
i
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e
c
h
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w
i
n
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w
i
t
h
i
n
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i
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a
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t
h
teeth closer to the jaw joint. In addition, a separate
examination of the in-lever for the temporalis based on
museum skulls of juveniles and adults showed that
adults have a greater mechanical advantage (Binder,
1998). Thus juvenile spotted hyenas seem to be at a
considerable disadvantage relative to adults.
Tooth development shows a distinct, two-step
process, with measures of tooth size (rst deciduous and
then permanent) increasing very rapidly as the teeth
emerged from the gum, followed by no change after
eruption was complete. The changeover from deciduous
to adult dentition took place between the ages of c. 12
and 14 months, beginning with the incisors, then the
carnassials, and nally the premolars and canines. The
permanent teeth were completely erupted by 14 months,
which is about 1 month earlier than has been docu-
mented in the wild (Kruuk, 1972; Mills, 1990).
Bite strength
Bite force improved gradually throughout the growing
period and continued past sexual maturity, which
occurs at c. 23 years of age for spotted hyenas (Frank,
Holekamp & Smale, 1995). Bite force showed some
potential for continued improvement even beyond
4 years of age, but changes beyond 5 years of age were
not statistically signicant.
Surprisingly, the increase in strength was apparently
not affected by the potentially disruptive replacement of
juvenile with adult dentition between 12 and 14 months
of age. During this time the jaw was growing, resulting
in a slow change in the position of all teeth relative to
the jaw joint, and therefore a shift in mechanical
advantage of the jaw muscles for each bite point
(Biknevicius, 1996). In addition, deciduous teeth were
being forced out slowly by emerging permanent teeth,
resulting in a mix of both types, and this probably
produced some malocclusion of teeth. Despite these
factors, there was no evidence that the process of tooth
replacement affected bite strength negatively, although
it may have been missed by this analysis if it were a very
brief phenomenon.
Interestingly, bite strength continued to increase
beyond the age at which skull growth seemed to have
stopped and the adult dentition was fully in place (i.e.
20 months of age) (Fig. 3a). It even continued well
beyond the point at which adult body sizes are reached
in the wild, between 24 and 36 months of age (Mills,
1990). This suggests that the jaw adductor musculature
continued to increase beyond the cessation of skeletal
growth. Our inability to detect this beyond 20 months
suggests that our external measurements were insuf-
cient. Zygomatic breadth only estimates one aspect of
jaw adductor muscle size, and other possible measures
such as development of sagittal and occipital crests were
difcult to assess. Notably, a recent morphometric
study of puma Puma concolor skulls demonstrated that
growth persisted throughout life (Gay & Best, 1996). It
would be useful to do a parallel study of spotted hyena
skulls of known age individuals but such samples are
rare.
Bite strength in individuals with newly erupted adult
teeth may have been restricted by the limited strength of
these teeth. When permanent teeth rst erupt, the thick-
ness of their pulp cavities is at a maximum, and over
time dentine is deposited and the pulp cavity narrows
with age (Tumlinson & McDaniel, 1984; Landon et al.,
1998). Therefore, a newly erupted permanent tooth may
be weaker than the same tooth later when it will have
more dentine. Consequently, bite strength may be con-
strained by tooth strength, which increases with age.
The bite strengths recorded for captive hyenas are
likely to be less than that of wild individuals because of
differences in diet and levels of competition. In addition
279 Bite strength and feeding in spotted hyenas
16
0.4
0.35
0.3
0.25
0.2
0.15
0.1
0.05
0
0 5 10 15 20 25 30
(a)
W
e
i
g
h
t

o
f

b
o
n
e

c
o
n
s
u
m
e
d

(
k
g
)
16
14
22 24 26 28 30
(b)
T
i
m
e

t
o

f
i
n
i
s
h

b
o
n
e

(
m
i
n
)
12
10
8
6
4
2
0
20 18
Age (months)
Fig. 5. (a) Amount of bone consumed in a 15 min `bone
crunching test,' showing an increase with increasing age.
Weight of bone consumed =0.056 +0.008 * age; r
2
=0.455,
Spearman rho =0.643, P<0.0001. (b) Time required to nish
bones (for cases in which bones were nished during the test)
for `bone crunching tests,' demonstrating a decrease with
age. Time to nish bone =17.094 0.338 * age; r
2
= 0.092,
Spearman rho =0.292, P<0.0739.
to not having to kill for themselves, the Berkeley hyenas
are fed a combination of small bones and ground meat,
both of which require much less strength to chew than
large bones and tougher food items such as skin and
cartilage. Moreover, they are fed regularly and mon-
itored to be certain each has eaten, which substantially
reduces competition during feeding. This might nega-
tively affect jaw muscle development, as well as the level
of motivation and aggression associated with feeding.
Finally, although no quantitative data are available, the
Berkeley hyenas seem to have smaller heads than their
wild counterparts (L. Frank, pers. comm.), suggesting
weaker development of the jaw adductor musculature,
probably as a result of the feeding regime. Conse-
quently, these bite force data should not be considered
as representative of the maximum capability of the
species in the wild.
Feeding behaviour and performance
The major change observed in feeding behaviour was
the shift in bone crunching from an emphasis on the
front to the back of the tooth row. It occurred gradually
between the ages of 4 and 20 months, with younger
individuals exhibiting much more variation in how they
fed. The rearward shift might be explained by altera-
tions in jaw muscle mechanics with growth that
favoured parallel changes in behaviour. As the jaw
grows, the deciduous carnassials and premolars are
replaced by permanent ones in slightly more posterior
positions relative to the jaw joint (Biknevicius, 1996).
Because the mechanical advantage of the jaw adductor
muscles tends to be greater for bites placed nearer the
jaw joint rather than farther away (Turnbull, 1970;
Hildebrand, 1988), the relative rearward movement of
the bone crunching teeth (premolars) shifts the teeth
into a more advantageous position, and the observed
change in feeding behaviour reected this. In our
sample, the use of anterior teeth dropped dramatically
after the adult teeth were fully erupted (c. 1214
months), suggesting that their arrival altered feeding
behaviour.
However, this does not explain why young juvenile
hyenas did not always use their rearmost premolars for
forceful biting. Indeed, Biknevicius (1996) determined
that the location of maximal bite force potential in the
juvenile hyena jaw was at the most posterior teeth, the
deciduous carnassials. Although her conclusions are
theoretically correct, the data presented here show an
opposing trend, where juveniles initially preferred to use
their front premolars, and shifted toward their rear
premolars as they aged.
Juveniles probably suffer from at least two con-
straints: (1) the need to protect the deciduous
carnassials from fracture; (2) limited gape size. Bone
crunching with the blade-like carnassials is likely to
blunt them at least, and fracture them at worst. Despite
the fact that deciduous teeth are temporary, selection
should favour retention of the only functional cutting
blades in the tooth row. Gape size is largely a function
of jaw length; the longer the jaws, the greater the size of
the object that can be placed between upper and lower
teeth. The smaller jaws of juvenile hyenas might not
have been capable of opening wide enough to accom-
modate a sheep femur between their rear teeth. They
were able to gradually position the bones more poster-
iorly in the region of near maximum bite force as the
constraints on gape size lessened with growth.
The change in feeding behaviour was accompanied by
improvements in feeding performance. In association
with their greater bite strength, older individuals tended
to consume more bone and consume it more rapidly
than younger individuals. Although performance
measures seemed to increase gradually with age, some
individuals exhibited a marked jump in speed of proces-
sing at 2022 months of age, the time when skull growth
reached a plateau. This followed by several months the
eruption of the adult teeth and subsequent emphasis of
rear premolars in feeding. This suggests that additional
bite strength was needed to achieve higher performance
levels. However, it is also possible that feeding beha-
viour may change due to learning. Feeding is an innate
behaviour, but effective and efcient feeding may
require experience (cf. Herring, 1985; Caro, 1994). The
potential effects of learning may be seen in the decrease
in variance of the measures of front premolar use with
age, signifying that more procient individuals spend a
greater percentage of time on certain types of feeding
techniques, whereas younger, less experienced indivi-
duals showed more variable behaviour. The need for
learning and experience in order to perform tasks
efciently has been noted in wild spotted hyenas, who
need years of practice of hunting to attain adult compe-
tency levels (often over 5 years; Holekamp, Smale, Berg
& Cooper, 1997).
Implications of our results for wild Crocuta
Our study of captive hyenas showed that the acquisition
of the adult dental battery did not coincide with either a
plateau in feeding performance or bite strength. By
around 2022 months of age, feeding behaviour was less
variable and skull growth was nearing its end. Never-
theless, strength continued to increase for several years
and speed of ingestion was still increasing at 30 months
of age when our study ended. What are the implications
of our results for wild spotted hyenas? To examine this,
we must review their life history.
Relative to other large carnivorans, spotted hyenas
and brown hyenas Hyaena brunnea have unusually
delayed average weaning times, nearly four times that of
similar-sized felids (Fig. 6). Data are not conclusive for
the striped hyena (Hyaena hyaena), but some sources
suggest that weaning times may be similar to that of
spotted and brown hyenas. The typical age of weaning,
12 months, coincides approximately with the acquisition
of adult dentition. This is not true of many or most
carnivorans, where weaning occurs well before this
W. 1. BiNnr :Nn B. V:N V:ixrNnicn 280
dental landmark (Table 3). In lions for example,
weaning age is typically 6 months whereas the adult
teeth are not in until the age of 1520 months (Schaller,
1972; Hillson, 1986). Similarly, wolves are weaned at
12 months, some 46 months before their adult teeth
have erupted (Mech, 1970). Biknevicius (1996) argued
that Crocuta delays weaning until the permanent teeth
are in because of the need to feed rapidly in competition
with conspecics over carcasses. Mills (1990) suggested
this as well and points out that unlike many other large
carnivorans, spotted hyenas rarely provision their
young with food, thus forcing the cubs to rely on their
mother's milk for longer. The absence of provisioning is
yet another by-product of their aggressive social feeding
behaviour; after a group of hyenas have fed, there is
usually little left for a female to bring home to her cubs.
Moreover, because Crocuta dens communally, the food
would be shared potentially with other cubs, especially
those that have inherited a high social rank from their
mothers (Mills, 1990).
Weaning age data for wild spotted hyenas suggest
that feeding competition is a signicant constraint on
juveniles. In a study of 53 juvenile Crocuta in the Masai
Mara, weaning ages ranged from 6.7 to 18.8 months
with most occurring around 12 months (Holekamp,
Smale & Szykman, 1996). High-ranking females weaned
their young earlier than low ranking females, probably
because they could guarantee their young access to kills
(van Lawick & van Lawick-Goodall, 1970; Hamilton,
Tilson & Frank, 1986; Holekamp, Smale & Szykman,
1996). In the Masai Mara study, low-ranking females
weaned their young slightly earlier when prey was
abundant, presumably because the increased food
supply resulted in decreased competition over carcasses
(Holekamp, Smale & Szykman, 1996). Clearly, there is a
tness advantage to the female of an earlier weaning
time because it reduces inter-birth interval length.
However, cubs weaned too early may starve in competi-
tion with adults.
Our study of captive hyena development suggests that
early weaning is a risky strategy and only possible for
mothers of relatively high rank. Before the eruption of
the adult dentition, feeding behaviour was highly
variable and bone crunching ability was quite limited. A
cub between the ages of 7 and 12 months would have
difculty dealing with the tougher parts of a carcass
(e.g. skin, bones), and probably would be restricted to
eating the more favoured parts, esh and organs. Unless
prey are exceptionally abundant, access to these is only
possible if the female can dominate the carcass, pre-
venting other adults from feeding. Low-ranked females
cannot do this, and thus it is critical that their cubs be
better equipped physically when they are weaned. Our
data from the captive hyenas indicated that signicant
improvements in bone crunching performance were
apparent 58 months after the typical weaning age of
12 months, probably as a result of both learning and
growth. Given this, a newly weaned 12- to 13-month-old
offspring of a low-ranking female would seem to be
especially vulnerable to starvation in the wild. There are
not yet sufcient eld data on mortality, age and social
rank to test this idea.
It is possible that rates of development in the eld
differ from those observed in the Berkeley colony. On
the one hand, the captives were well-fed, and this might
result in faster development. On the other hand, post-
weaning development of jaw strength in the wild might
occur more rapidly simply because of the greater
demands placed on the masticatory system. Young
hyenas must compete side-by-side with others for food,
and speed of ingestion is critical. In their struggles to
feed, wild hyenas are likely to load their muscles and
bones heavily, and this should lead to a rapid acquisi-
tion of strength. By contrast, there was no change in the
food type or quantity in the captive sample throughout
the study and hence strength acquisition may have
281 Bite strength and feeding in spotted hyenas
Table 3. Age at weaning and age where adult dentition is complete for several large carnivorans
Species Weaning age (months) Adult teeth complete (months) References
Canis lupus, grey wolf 12 46 Mech, 1970; Gittleman, 1986
C. familiaris, domestic dog 1 67 Hillson, 1986; Evans, 1993
Vulpes vulpes, red fox 2 46 Gittleman, 1986; Hillson, 1986
Panthera leo, African lion 6 1520 Schaller, 1972; Hillson, 1986
Felis catus, domestic cat 2 67 Gittleman, 1986; Hillson, 1986
Crocuta crocuta, spotted hyena 1215 1214 Kruuk, 1972; Mills 1990
Hyaena brunnea, brown hyena 912 1214 Mills, 1990
CC
HB
180 160 140 120 100 80 60 40 20 0
0
50
100
150
200
250
300
350
400
W
e
a
n
i
n
g

a
g
e

(
d
a
y
s
)
Body mass (kg)
Fig. 6. Weaning as a function of body mass for several species
within the Carnivora; Weaning age (days) =81.652 +.782*
body mass (kg); r
2
=0.153. CC, Crocuta crocuta; HB, Hyaena
brunnea.
occurred more gradually. In any case, it would be
interesting to know whether speed of ingestion, less
variable feeding behaviour, and near cessation of skull
growth were all associated in the wild as they were in
our captive sample.
The brown hyena also has a late weaning time
relative to other carnivorans (Fig. 6), which suggests
that food competition might not be the sole reason for
the delay. Brown hyenas exist in small extended family
groups but usually forage on their own, customarily
scavenging opportunistically, preying on small verte-
brates and consuming some fruits (Mills, 1990). Cubs
are provisioned with food beginning at c. 4 months of
age, and consequently are less reliant on suckling than
are spotted hyena cubs. Nevertheless, brown hyena
cubs are weaned only slightly earlier, at c. 912 months
of age (Mills, 1990). Perhaps the delayed weaning age
reects limits on how rapidly the transition from cub to
adult skull morphology can occur. Brown hyenas have
skulls and teeth that are nearly as massive as those of
spotted hyenas (Ewer, 1973; Radinsky, 1981; Van Valk-
enburgh, 1989). The developmental transformation that
takes place in spotted and brown hyenas is profound, if
only because of the relatively large size of the adult
teeth which must be housed in the skull and jaws
(cf. Biknevicius & Leigh, 1997). Perhaps, this transfor-
mation requires more compromise in feeding
performance than is typical of other carnivorans where
weaning occurs well before the adult teeth are in place.
Consequently, brown and spotted hyena cubs might
not be able to survive easily on adult foods and are
therefore dependent on their mothers for an extended
period.
Clearly, our understanding of the possible constraints
on weaning age, dental eruption time, and the develop-
ment of feeding prociency in hyenas would benet
from comparable data on other species. Even though
juvenile deaths are a major contributor to overall mor-
tality in most carnivorans, relatively little attention has
been paid to the lives of juveniles and their adaptations
for survival. Although eld data might be preferred,
studies on captive hyenas are benecial and provide
hypotheses to be tested in the eld.
Acknowledgements
We thank Kathleen Green and Jon Cano for assistance
with data collection, and Steve Glickman, Laurence
Frank, Mary Weldele, Christine Drea and Elizabeth
Coscia for their encouragement and advice at the
Berkeley Field Station. We thank Dean Dessem and Jeff
Thomasen for advice on the design of the bite force
device. We also thank David Jacobs, Tom Plummer and
Fritz Hertel for their comments and suggestions.
Finally, we thank two anonymous reviewers for their
helpful comments. This study was supported by the
University of California Academic Senate and the
Malcolm Stacey Fund (University of California Ofce
of the President).
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283 Bite strength and feeding in spotted hyenas