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Bite strength is of great importance to carnivores, as their jaws must produce forces of suf(r)cient magnitude to kill and consume their prey. Nine captive individuals, aged 6 months to 2 years of age, were sampled as they grew. A fundamental change in tooth use during bone cracking followed the replacement of deciduous teeth with permanent teeth.
Bite strength is of great importance to carnivores, as their jaws must produce forces of suf(r)cient magnitude to kill and consume their prey. Nine captive individuals, aged 6 months to 2 years of age, were sampled as they grew. A fundamental change in tooth use during bone cracking followed the replacement of deciduous teeth with permanent teeth.
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Bite strength is of great importance to carnivores, as their jaws must produce forces of suf(r)cient magnitude to kill and consume their prey. Nine captive individuals, aged 6 months to 2 years of age, were sampled as they grew. A fundamental change in tooth use during bone cracking followed the replacement of deciduous teeth with permanent teeth.
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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) 325 300 275 250 225 200 175 150 125 100 75 50 5 0 5 10 15 20 25 30 35 40 H e a d
m e a s u r e m e n t s
( m m ) 5 0 5 10 15 20 25 30 35 40 18 16 14 12 10 8 6 4 2 0 T o o t h
m e a s u r e m e n t s
( m m ) 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 4500 4000 3500 3000 2500 2000 1500 1000 500 0 500 0 20 40 60 100 120 140 160 180 B i t e
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( N ) 80 1400 1200 1100 800 600 400 200 0 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 e n t
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t o o t h
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( % ) 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 e o f t i m e c h e w i n g w i t h i n d i c a t e d t e e 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
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( k g ) 16 14 22 24 26 28 30 (b) T i m e
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( 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. 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