The effects of gape angle and bite point on bite force in bats
1 Department of Biology, University of Massachusetts-Amherst, Morrill
Science Center, 611 North Pleasant Street, Amherst, MA 01003-9297,
USA
2 Laboratory of Functional Morphology, Department of Biology, University of
Antwerp, Universiteitsplein 1, B-2610 Antwerpen, Belgium
* Author for correspondence (e-mail: bdumont{at}bio.umass.edu)
Accepted 17 March 2003
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Summary |
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Key words: bat, bite force, gape, behavior, performance
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Introduction |
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Despite the widespread use of these models and predictions in discussions
of mammalian feeding (e.g. Carraway et al.,
1996; Dumont, 1997
;
Emerson and Radinsky, 1980
;
Freeman, 1981
;
Kiltie, 1982
;
Perez-Barberia and Gordon,
1999
; Reduker,
1983
; Sicuro and Oliveira,
2002
; Stafford and Szalay,
2000
), there are surprisingly few experimental data documenting
bite force in non-human mammals. Data summarizing maximum bite forces elicited
using electrical stimulation are available for macaques, opossums, and rats
(Dechow and Carlson, 1983
;
Robins, 1977
;
Thomason et al., 1989
).
Natural, non-stimulated bite forces have been recorded at single (or combined)
bite points in possums, hyenas, ferrets and bats
(Aguirre et al., 2002
;
Binder and Van Valkenburgh,
2000
; Dessem and Druzinsky,
1992
; Thomason et al.,
1989
). Variation in non-stimulated bite force has been reported
only for galagos and macaques (Hylander,
1977
,
1979
), in which there is a
positive relationship between bite force and increasingly posterior bite
point.
Humans are the only mammals in which the combined effects of gape and bite
point on non-stimulated bite force production have been studied in any detail.
Even so, the integrated effects of bite point and gape angle on force
production remain unclear (Spencer,
1999). Among experiments in which gape and bite point are altered
simultaneously, bite force is reported either to increase posteriorly
(Mansour and Reynick, 1975
;
Oyen and Tsay, 1991
) or to
peak at the first molar and then decrease
(Pruim et al., 1980
). A
similar inference was drawn by Spencer
(1998
), based on associations
between muscle activity and bite point. One study reports that when gape angle
is held constant, unilateral bite force increases from canine to second molar
positions (van Eijden, 1991
).
In contrast, when bite point is held constant and gape is varied, there
appears to be an optimum gape angle at which maximum forces are produced
(Fields et al., 1986
;
Mackenna and Turker, 1983
;
Manns et al., 1979
). The
combination of varying results from human studies and lack of experimental
data from non-human mammals leaves the relationship between gape angle, bite
point and bite force unresolved. With this study, our goal is to document
variation in non-stimulated bite force that is associated with changes in gape
angle and bite point in a single group of mammals.
Bats are optimal subjects for evaluating the functional relationships among
gape angle, bite point and bite force. While the skulls of bats are
morphologically diverse, the masticatory apparatus is not so highly derived as
to preclude them from being a good model for generalized mammals (e.g.
Dumont, 1997; Freeman,
1981
,
1988
,
2000
). Evidence from one
species (Pteropus giganteus) demonstrates a pattern of muscle
activity during mastication that is common to many mammals
(De Gueldre and De Vree, 1988
;
Hylander et al., 2000
;
Langenbach and van Eijden,
2001
). In addition, bats exhibit inter-specific variation in bite
force (Aguirre et al., 2002
),
species-specific variation in preferred bite points during feeding
(Dumont, 1999
;
Dumont and O'Neal, in press
),
and they eat foods that cover a wide range of size and hardness values
(Dumont, 2003
). The rapidly
growing base of information about the size and hardness of foods that bats eat
facilitates a priori predictions about feeding performance,
morphology and feeding behavior, making bats an excellent group in which to
study mammalian feeding.
Here we use three separate data sets collected from plant-visiting bats to
investigate the dual impacts of gape angle and bite point on bite force. To
study the relationship between gape angle and bite force across species, we
assembled data summarizing bite force and gape angle during bilateral canine
biting for 11 bat species and tested the prediction that there is a
significant negative association between gape angle and bite force across
species. The relationship between gape angle and bite force within species was
investigated using a second dataset containing bite forces measured at the
same bite point but at increasing gape angles within each of four species.
Finally, to test the prediction that bite force increases at progressively
posterior bite points, we assembled a third data set documenting relative
force during unilateral canine and molar biting in seven species in which gape
angle increases only slightly from anterior to posterior bite points. During
feeding, bats are known to use both unilateral and bilateral canine biting
(Dumont, 1999;
Dumont and O'Neal, in press
).
To evaluate the functional implications of symmetrical and asymmetrical canine
loading, we also collected unilateral canine bite force for these same seven
species.
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Materials and methods |
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Bite forces were measured using a piezzo electric force transducer
(Kistler, type 9203, range ±500 N; Amherst, NY, USA) attached to a
handheld charge amplifier (Kistler, type 5995). The transducer is linear
across its entire range. Coupled with the charge amplifier, it measures forces
at the low end of the sensitivity range with an accuracy of 0.01 N, and at the
high end of the sensitivity range with an accuracy of only 0.1 N. Thus the
accuracy of the force readings is proportional to the magnitude of the forces.
The transducer was mounted between two bite plates as described and
illustrated in Herrel et al.
(1999) and Aguirre et al.
(2002
). The distance between
the bite plates was varied for different species to adjust gape angles. Using
the known distance between the bite plates and the location of the bite point,
we calculated gape angles for each species using digital pictures of dry
skulls from museum collections. Given a distance between upper and lower
teeth, gape angle was measured as the angle subtended by the lines connecting
the temporomandibular joint to the tips of the upper and lower canines or
first molars.
Bats were usually eager to bite the transducer, and were stimulated to bite by gentle taps at the side of mouth if needed. To protect the bats' teeth and to provide a non-skid surface, the tips of the bite plates were covered with a layer of cloth medical tape. At least five trials were recorded for each individual at each bite position and/or gape angle (note that a single trial can, and usually did, consist of multiple bites). The trial that produced the strongest bite appeared to be random, suggesting that the animals were not accommodating to the texture of the bite plates as the trials progressed. Animals were allowed to rest for at least 20 min between successive trials. The maximal bite force obtained during the trials was considered the maximal bite force for that individual. Many of the bites consisted of repeated `clenching' of the bite plates between bats' teeth. However, it is important to point out that the bites in this study are most accurately described as defensive and may not reflect bite forces generated during unrestrained feeding. Average bite forces were calculated for each species. Immediately following the collection of bite force data, animals were measured (head length, width, height), weighed and released.
We evaluated the relationship between gape angle and bite force in two ways
and with two separate data sets. First, we compared the forces generated
during bilateral canine biting at different gape angles across 11 species of
bats (Table 1). Because bite
force scales with body size (Aguirre et
al., 2002; Herrel et al.,
2002
,
2001
,
1999
,
1996
), we regressed the
maximal bite force for each species against a series of size estimates
[ln(body mass), (body mass)2/3, head length, (head
length)2, head width, head height, head widthxheight, (head
volume)1/3] to identify the one with the greatest explanatory
power. Head length explained the greatest proportion of the variation in bite
force (r2=0.902, compared to a maximum of
r2=0.855 for a body mass variable) and residuals were
extracted from a regression of bite force on head length. These residual (i.e.
size-adjusted) bite forces were then regressed against gape angle using
least-squares techniques (Sokal and Rohlf,
1995
).
Second, we evaluated the effect of gape angle on bite force during
bilateral canine biting for five individuals each of Rousettus
aegyptiacus, Cynopterus brachyotis, Artibeus jamaicensis and Pteropus
poliocephalus. For each species the bite plates were set at different
distances, thus inducing variation in gape angle. The difference in angle
between the lowest and highest gape positions ranged from 22° to 33°.
The effect of species and bite point on bite force was investigated using a
two-way, repeated-measures analysis of variance test (ANOVA)
(Sokal and Rohlf, 1995).
To investigate the relationship between the point of application of bite
force along the tooth row (bite point) and bite force, we assembled a third
data set containing bite force measurements collected from three different
bite points in seven bat species. The bite points included bilateral canine
biting, unilateral canine biting and unilateral molar biting. These bite
positions were chosen as they reflect the natural variation in bite points
observed in unrestrained feeding trials in bats (Dumont,
1999,
2003
;
Dumont and O'Neal, in press
).
Data from these bite points allowed us to evaluate simultaneously the effects
of anterior versus posterior bite placement and symmetrical and
asymmetrical loading of the canines. To collect these data, the distance
between the bite plates was set so that gape angle varied by less than 12°
between canine and molar bite points and thus minimized potential gape
effects. To control the effect of inter-specific variation in body size on
absolute bite force, bite force within each species was expressed relative to
its maximal bite force. A single classification ANOVA and post-hoc
multiple-comparisons test was used to document differences in relative bite
force between bite positions across species. All analyses were performed using
SPSSTM (Version 10, Chicago, IL, USA).
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Results |
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All species exhibit a substantial increase in relative bite force as animals shift from unilateral canine biting to unilateral molar biting (Fig. 3). Molar biting consistently produces the highest bite forces while unilateral canine biting universally results in the lowest forces. Pteropus poliocephalus is unique in producing very similar forces during bilateral and unilateral canine biting. Across species, relative bite force differs significantly among the three bite positions (F(2,18)=23.40, P<0.001) and between all pairs of bite positions (Tukey's HSD test, P<0.05 in all comparisons). Untransformed bite forces and gape angles for these seven species are presented in Table 2.
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Discussion |
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Variation among species in their motivation to bite the apparatus may
explain some of the scatter in this regression. Although we could not discern
clear interspecific differences in behavior, this potential source of
variation cannot be ruled out and, indeed, must be accepted in exchange for
voluntary (non-stimulated) bite force data. The fact that these species
exhibit a wide variety of cranial shapes is another factor that may underlie
the scatter in this regression. Although the bite forces used in this
inter-specific regression are size-adjusted, they are not shape-adjusted.
Among humans, subtle differences in absolute bite force production have been
associated with variation in face shape
(Proffit et al., 1983). The
cranial morphology of bats is extremely diverse, even among plant-visiting
species (Dumont, 1997
;
Freeman, 1988
;
Storch, 1968
). It is likely
that architectural details of the skull, including muscle size, muscle fiber
orientation and bony morphology, contribute to variation in bite force. Based
on skull anatomy alone it is not clear why Eidolon helvum, Pteropus
vampyrus and Pteropus poliocephalus are outliers in this
analysis. However, the anatomy of the masticatory musculature is unknown for
these species and may have a critical influence on their ability to produce
bite forces.
The influence of gape angle on bite force is underscored by intra-specific comparisons (Fig. 2), where again there is a significant trend toward decreased bite force with increasing gape angle. Among these species, P. poliocephalus is unique in exerting equal bite forces at medium and high gape angles. One possible explanation is that the change in gape angle between medium and high gape was less in P. poliocephalus than in other species (9° versus 1516°). The smaller change in angle, and consequent lower gape angle during biting at a wide gape, may have moderated the effect of gape on bite force at the widest gape position. In addition, P. poliocephalus was the most aggressive species that we sampled and appeared to be highly motivated to bite.
Finally, the shape of the bony skull and dentary in P. poliocephalus differs substantially from that of Artibeus jamaicensis, Cynopterus brachyotis, and Rousettus aegyptiacus. Relative to these other species, P. poliocephalus may be optimized for strong biting at high gape angles. Additional data documenting muscle size and orientation, bite force and feeding behavior in this and other species of Pteropus are needed to fully investigate these alternatives.
With respect to unilateral canine versus molar biting, regardless of body size, maximum bite forces are produced during unilateral molar biting. Across species, forces produced during unilateral canine biting vary between 30% and roughly 70% of those produced during unilateral molar biting. The pattern of variation among species does not track differences in body size, dietary habits or family membership. Again we suggest that the relationship between interspecific variation in patterns of bite force production and variation in bony and muscular architecture deserves further investigation. Despite variation in the relative magnitude of unilateral canine bite forces, the overall pattern of higher bite force during unilateral molar biting accords well with the general prediction of both constrained and unconstrained lever models of the mammalian masticatory apparatus that bite force increases as bite point shifts posteriorly. Testing the detailed predictions of these models (i.e. that bite force increases incrementally or that it peaks near the first molar and then decreases or remains constant at second and third molar positions) can only be accomplished with bite force data from each tooth position within the post-canine tooth row.
The fact that forces generated during unilateral canine biting are almost
universally lower than forces generated during bilateral canine biting
suggests that there is a constraint on unilateral canine bite force
production. There are at least two potentially limiting factors. First, the
decreased forces produced during unilateral canine biting may be a means of
protecting the canines from damage. During bilateral canine biting the force
of biting is spread across the tips of all four canines. In contrast, the
force of biting is concentrated on the tips of only two canines during
unilateral canine biting. If equal forces were generated in both unilateral
and bilateral canine biting, the canine teeth involved in unilateral biting
would experience much higher concentrations of stress. In contrast to the
canines of carnivorans, the canine teeth of bats are relatively long, thin and
exhibit sharp crests along their length
(Freeman, 1992). While this
morphology may enhance the ability of these teeth to initiate and propagate
cracks in food items (Freeman,
1992
), it is not well suited to resist breaking under high loads
(Van Valkenburgh and Ruff,
1987
). Given the shape of bat canine teeth and the concentration
of forces on fewer teeth during unilateral biting, we suggest that sensory
feedback from the canine alveoli may serve as a signal to decrease bite force
during unilateral canine biting and thus protect these teeth from high
stresses and potential damage. A detailed investigation of canine shape and
relative bite force during unilateral and bilateral loading would be a
reasonable first step toward testing this hypothesis.
A second factor that could serve to constrain force production during
unilateral canine biting is the twisting of the face that would result from
high unilateral forces applied near the front of the mouth. With respect to
the skeleton of the lower face, unilateral loading during mastication (i.e.
unilateral molar biting) in primates produces patterns of strain consistent
with torsion (e.g. Ravosa et al.,
2000; Ross, 2001
;
Ross and Hylander, 1996
). By
extension, unilateral canine biting is also likely to result in twisting of
the facial skeleton. Relative to the molar teeth, the greater distance of the
canine from the temporomandibular joint may even exaggerate twisting strains.
All other things being equal, unilateral canine biting forces equal to those
produced during bilateral canine biting could produce a much higher strain
than that imposed by unilateral molar activity during mastication. Although
safety factors in the facial skeleton appear to be quite high
(Hylander and Johnson, 1997
),
it remains a possibility that bite forces (at all bite points) are modulated
via proprioceptive feedback from regions of the facial skeleton
experiencing strain. Strain analysis of the bat facial skeleton during feeding
would constitute a first step toward evaluating this hypothesis.
Interestingly, differences in unilateral and bilateral canine bite forces are
not associated with gross variation in the morphology of the lower jaw.
Although we sampled only one species with an unfused symphysis
(Phyllostomus hastatus), the relative magnitudes of unilateral and
bilateral bite forces do not appear to differ between this species and the
others in the sample.
Variation in bite force production between symmetrical and asymmetrical
loading is an interesting issue that has received very little attention. In
contrast to the data reported here, the only other studies comparing
unilateral and bilateral biting report that bite forces are equal during
unilateral and bilateral molar biting in humans
(Mansour and Reynick, 1975;
van Eijden, 1991
). Whether the
same is true during unilateral and bilateral molar biting in bats and whether
there are differences in bite force during unilateral and bilateral canine
biting in humans is not known. We are currently designing modified bite plates
to gather these data.
Overall, the data presented here constitute the most comprehensive
assessment of variation in bite force available for mammals and support
existing models of bite force production in species with generalized cranial
morphology. Both bite point and gape angle significantly impact bite force.
The interaction between these two variables has important implications for
ecomorphological analyses of feeding in mammals. From an ecomorphological
perspective, bite force provides a measure of feeding performance because it
circumscribes the range of food items that animals can use
(Aguirre et al., 2002;
Binder and Van Valkenburgh,
2000
). Mammals use many different, species-specific combinations
of bite points and gape angles during feeding
(Dumont, 1999
;
Dumont, 2003
;
Dumont and O'Neal, in press
;
Van Valkenburgh, 1996
). The
data presented here suggest that it is important to account for behavioral
variation if the goal is to make ecologically relevant functional comparisons
among species. These data also highlight interspecific differences in bite
force production that are likely to be associated with variation in the bony
and muscular architecture of the masticatory system. The evolutionary
relationships between bite force, feeding behavior and craniofacial morphology
are intriguing avenues of research that have the potential to highlight
patterns of adaptation and constraint in the evolution of feeding in
mammals.
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Acknowledgments |
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References |
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Aguirre, L. F., Herrel, A., van Damme, R. and Matthysen, E. (2002). Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community. Proc. R. Soc. Lond. B 269,1271 -1278.[CrossRef][Medline]
Binder, W. J. and Van Valkenburgh, B. (2000). Development of bite strength and feeding behaviour in juvenile spotted hyenas (Crocuta crocuta). J. Zool. 252,273 -283.[CrossRef]
Carraway, L. N., Verts, B. J., Jones, M. L. and Whitaker, J. O. (1996). A search for age-related changes in bite force and diet in shrews. Amer. Midland Nat. 135,231 -240.
De Gueldre, G. and De Vree, F. (1988). Quantitative electromyography of the masticatory muscles of Pteropus giganteus (Megachiroptera). J. Morphol. 196,73 -106.[Medline]
Dechow, P. C. and Carlson, D. S. (1983). A method of bite force measurement in primates. J. Biomech. 16,797 -802.[Medline]
Dessem, D. and Druzinsky, R. E. (1992). Jaw muscle activity in ferrets, Mustela putorius furo. J. Morphol. 213,275 -286.[Medline]
Dumont, E. R. (1997). Cranial shape in fruit, nectar, and exudate feeders: Implications for interpreting the fossil record. Am. J. Phys. Anthropol. 102,187 -202.[CrossRef][Medline]
Dumont, E. R. (1999). The effect of food hardness on feeding behaviour in frugivorous bats (Phyllostomidae): An experimental study. J. Zool., Lond. 248,219 -229.
Dumont, E. R. (2003). Bats and fruit: an ecomorphological approach. In Bat Ecology (ed. T. H. Kunz and M. B. Fenton), pp. 398-429. Chicago: University of Chicago Press.
Dumont, E. R. and O'Neal, R. (in press). Food hardness and feeding behavior in Old World fruit bats. J. Mammal.
Emerson, S. B. and Radinsky, L. B. (1980). Functional analysis of sabertooth cranial morphology. Paleobiol. 6,295 -312.
Fields, H. W., Proffitt, W. R., Case, J. C. and Vig, K. W. L. (1986). Variables affecting measurements of vertical occlusal force. J. Dental Res. 62,135 -138.
Freeman, P. W. (1981). Correspondence of food habits and morphology in insectivorous bats. J. Mammal. 62,166 -173.
Freeman, P. W. (1988). Frugivorous and animalivorous bats (Microchiroptera) dental and cranial adaptations. Biol. J. Linn. Soc. 33,249 -272.
Freeman, P. W. (1992). Canine teeth of bats (Microchiroptera): size, shape and role in crack propagation. Biol. J. Linn. Soc. 45,97 -115.
Freeman, P. W. (2000). Macroevolution in microchiroptera: recoupling morphology and ecology with phylogeny. Evol. Ecol. Res. 2,317 -335.
Greaves, W. S. (1978). The jaw lever system in ungulates: A new model. J. Zool., Lond. 184,271 -285.
Herrel, A., De Grauw, E. and Lemos-Espinal, J. A. (2001). Head shape and bite performance in xenosaurid lizards. J. Exp. Zool. 290,101 -107.[CrossRef][Medline]
Herrel, A., O'Reilly, J. C. and Richmond, A. M. (2002). Evolution of bite performance in turtles. J. Evol. Biol. 15,1083 -1094.[CrossRef]
Herrel, A., Spithoven, L., Van Damme, R. and De Vree, F. (1999). Sexual dimorphism of head size in Gallotia galloti: Testing the niche divergence hypothesis by functional analyses. Funct. Ecol. 13,289 -297.[CrossRef]
Herrel, A., Van Damme, R. and De Vree, F. (1996). Testing the niche divergence hypothesis by bite force analysis. Neth. J. Zool. 46,253 -262.
Herring, S. W. and Herring, S. E. (1974). The superficial masseter and gape in mammals. Amer. Nat. 108,561 -576.[CrossRef]
Hylander, W. L. (1975). The human mandible: lever or link? Am. J. Phys. Anthropol. 43,227 -242.[Medline]
Hylander, W. L. (1977). In vivo bone strain in the mandible of Galago crassicaudatus. Am. J. Phys. Anthropol. 46,309 -326.[Medline]
Hylander, W. L. (1979). Mandibular function in Galago crassicaudatus and Macaca fasicularis: An in vivo approach to stress analysis of the mandible. J. Morphol. 159,253 -296.[Medline]
Hylander, W. L. and Johnson, K. R. (1997). In vivo bone strain patterns in the zygomatic arch of macaques and the significance of these patterns for functional interpretations of craniofacial form. Am. J. Phys. Anthropol. 102,203 -232.[CrossRef][Medline]
Hylander, W. L., Ravosa, M. J., Ross, C. F., Wall, C. E. and Johnson, K. R. (2000). Jaw-muscle recruitment patterns during mastication in anthropoids and prosimians. Am. J. Phys. Anthropol. 112,469 -492.[CrossRef][Medline]
Kiltie, R. A. (1982). Bite force as a basis for niche differentiation between rain forest peccaries (Tayassu tajacu and T. pecari). Biotropica 14,188 -195.
Langenbach, G. E. J. and van Eijden, T. (2001). Mammalian feeding motor patterns. Am. Zool. 41,1338 -1351.
Lindauer, S. J., Gay, T. and Rendell, J. (1993). Effect of jaw opening on masticatory muscle EMG-force characteristics. J. Dental Res. 72, 51-55.[Abstract]
Mackenna, B. R. and Turker, K. S. (1983). Jaw separation and maximum incising force. J. Pros. Dent. 49,726 -730.
Manns, A., Miralles, R. and Palazzi, C. (1979). EMG, bite force, and elongation of masseter muscle under isometric voluntary contractions of the human masseter muscle. J. Pros. Dent. 42,674 -682.
Mansour, R. M. and Reynick, R. J. (1975). In vivo occlusal forces and moments: I, Forces measured in terminal hinge position and associated moments. J. Dental Res. 54,114 -120.[Abstract]
Oyen, O. J. and Tsay, T. P. (1991). A biomechanical analysis of craniofacial form and bite force. Am. J. Orthodont. Dentofacial Orthoped. 99,298 -309.
Perez-Barberia, F. J. and Gordon, I. J. (1999). The functional relationship between feeding type and jaw and cranial morphology in ungulates. Oecologia 118,157 -165.[CrossRef]
Proffit, W. R., Fields, H. W. and Nixon, W. L. (1983). Occlusal forces in normal and long-face adults. J. Dental Res. 62,566 -571.[Abstract]
Pruim, G. J., De Jongh, H. J. and Ten Bosch, J. J. (1980). Forces acting on the mandible during bilateral static biting at different bite force levels. J. Biomech. 13,755 -763.[Medline]
Radinsky, L. B. (1981). Evolution of skull shape in carnivores 1. representative modern carnivores. Biol. J. Linn. Soc. 15,369 -388.
Ravosa, M. J., Johnson, K. R. and Hylander, W. L. (2000). Strain in the galago facial skull. J. Morphol. 245,51 -66.[CrossRef][Medline]
Reduker, D. W. (1983). Functional analysis of the masticatory apparatus in two species of Myotis. J. Mammal. 64,277 -286.
Robins, M. W. (1977). Biting loads generated by the laboratory rat. Arch. Oral Biol. 22, 43-47.[Medline]
Ross, C. F. (2001). In vivo function of the craniofacial haft: The interorbital `pillar'. Am. J. Phys. Anthropol. 116,108 -139.[CrossRef][Medline]
Ross, C. F. and Hylander, W. L. (1996). In vivo and in vitro bone strain in the owl monkey circumorbital region and the function of the postorbital septum. Am. J. Phys. Anthropol. 101,183 -215.[CrossRef][Medline]
Sicuro, F. L. and Oliveira, L. F. B. (2002). Coexistence of peccaries and feral hogs in the Brazilian pantanal wetland: An ecomorphological view. J. Mammal. 83,207 -217.
Sokal, R. R. and Rohlf, F. J. (1995). Biometry: The Principles and Practice of Statistics in Biological Research: W. H. Freeman and Company.
Spencer, M. A. (1998). Force production in the primate masticatory system: Electromyographic tests of biomechanical hypotheses. J. Hum. Evol. 34, 25-54.[CrossRef][Medline]
Spencer, M. A. (1999). Constraints on masticatory system evolution in anthropoid primates. Am. J. Phys. Anthropol. 108,483 -506.[CrossRef][Medline]
Stafford, B. J. and Szalay, F. S. (2000). Craniodental functional morphology and taxonomy of dermopterans. J. Mammal. 81,360 -385.
Storch, G. (1968). Funktionsmorphologische Untersuchungen an der Kaumuskulatur und an kerrelierten schadelstrukturen der chiropteren. Abh. Senckenberg. Natur. Gesell. 51, 1-92.
Thomason, J. J., Russell, A. P. and Morgeli, M. (1989). Forces of biting, body size, and masticatory muscle tension in the opossum Didelphis virginiana. Can. J. Zool. 68,318 -324.
Turkawski, S. J. J. and van Eijden, T. (2001). Mechanical properties of single motor units in the rabbit masseter muscle as a function of jaw position. Exp. Brain Res. 138,153 -162.[CrossRef][Medline]
van Eijden, T. M. G. J. (1991). Three-dimensional analyses of human bite-force magnitude and moment. Arch. Oral Biol. 36,535 -539.[Medline]
Van Valkenburgh, B. (1996). Feeding behavior in free-ranging large African carnivores. J. Mammal. 77,240 -254.
Van Valkenburgh, B. and Ruff, C. B. (1987). Canine tooth strength and killing behavior in large carnivores. J. Zool., Lond. 212,379 -397.
Weishampel, D. B. (1993). Beams and machines: modeling approaches to the analysis of skull form and function. In The Skull: Functional and Evolutionary Mechanisms, vol. 1 (ed. J. Hanken and B. K. Hall), pp.303 -344. Chicago: University of Chicago Press.