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Differentiation of craniomandibular morphology in two sympatric Peromyscus mice (Cricetidae: Rodentia)

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Abstract

In the Santa Cruz Mountains of California, dietary partitioning is believed to allow Peromyscus californicus (California mouse) and Peromyscus truei (pinyon mouse) to occur sympatrically; P. californicus feeds primarily on arthropods, whereas P. truei feeds primarily on acorns. To better understand how these species partition resources, we examine if these dietary differences extend to differences in craniomandibular morphology. We use a geometric morphometric approach to test the hypothesis that P. californicus and P. truei exhibited size and shape differences in craniomandibular morphology, in particular, regions of the skulls that pertain to biting ability and mechanical advantage of the jaw adductor muscles. We found that P. truei exhibited relatively wider zygomatic arches, relatively broader, more robust masseteric fossa and coronoid process, and a higher mechanical advantage of the masseter jaw muscle. These craniomandibular traits suggested that P. truei exhibits a relatively stronger bite force that is more suitable to access hard-shelled acorns despite its smaller body size.
ORIGINAL PAPER
Differentiation of craniomandibular morphology in two sympatric
Peromyscus mice (Cricetidae: Rodentia)
Kaz Jones
1
&Chris J. Law
1
Received: 20 December 2017 /Accepted: 8 March 2018
#Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2018
Abstract
In the Santa Cruz Mountains of California, dietary partitioning is believed to allow Peromyscus californicus (California mouse)
and Peromyscus truei (pinyon mouse) to occur sympatrically; P. californicus feeds primarily on arthropods, whereas P. truei
feeds primarily on acorns. To better understand how these species partition resources, we examine if these dietary differences
extend to differences in craniomandibular morphology. We use a geometric morphometric approach to test the hypothesis that
P. californicus and P. truei exhibited size and shape differences in craniomandibular morphology, in particular, regions of the
skulls that pertain to biting ability and mechanical advantage of the jaw adductor muscles. We found that P. truei exhibited
relatively wider zygomatic arches, relatively broader, more robust masseteric fossa and coronoid process, and a higher mechan-
ical advantage of the masseter jaw muscle. These craniomandibular traits suggested that P. truei exhibits a relatively stronger bite
force that is more suitable to access hard-shelled acorns despite its smaller body size.
Keywords Bite force .Dietary partitioning .Geometric morphometrics .Mechanical advantage .Skull morphology
Introduction
Closely related species often share morphological and func-
tional characteristics that allow them to fall within the same
ecological guild and use the same resources in similar ways
(Root 1967; Schoener 1974; Dayan and Simberloff 1994).
However in zones of sympatry, high interspecific competition
is expected to drive resource partitioning between these eco-
logically similar species resulting in separation of ecological
niches such as space use, time, and/or diet (Pianka 1973;
Schoener 1974). Accompanying niche partitioning is differ-
entiation of the underlying morphology/physiology, behavior,
and performance that facilitates exploitation of specific re-
sources for each species (Verwaijen et al. 2002; Mori and
Vincent 2008;Žagar et al. 2017). This ecomorphological par-
adigm elucidates the interactions between sympatric species
and their environments (Wainwright 1991; Ferry-Graham
et al. 2002; Grant and Grant 2002), which in turn provides
better understanding of the mechanisms that shape species
coexistence.
As the most populous native mammals in North America,
deer mice (genus Peromyscus) range across a variety of eco-
systems and frequently share overlapping habitats between
two or three Peromyscus species (Kaufman and Kaufman
1989). Extensive studies on niche partitioning between sym-
patric deer mice have found that differences in dietary prefer-
ence may be one of the primary mechanisms that reduce in-
terspecific competition (Smartt 1978; Kalcounis-Rüppell and
Millar 2002;Reidetal.2013). Researchers have also exam-
ined the morphological, behavioral, and functional differences
that underlie differences in the exploitation of prey. In most
mammals, the ability to exploit particular prey is limited by
the biting ability generated by craniomandibular morphology
(Kardong 2014). Therefore, the ecomorphological paradigm
hypothesizes a strong link between craniomandibular mor-
phology and prey exploitation. Previous studies with lizards,
turtles, birds, and mammals have revealed that variation in
craniomandibular morphology can influence dietary profit-
ability by expanding/limiting the food items accessible to a
Communicated by: Joanna Stojak
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s13364-018-0364-2) contains supplementary
material, which is available to authorized users.
*Chris J. Law
cjlaw@ucsc.edu
1
Department of Ecology and Evolutionary Biology, University of
California, Coastal Biology Building, Santa Cruz, 130 McAllister
Road, Santa Cruz, CA 95060, USA
Mammal Research
https://doi.org/10.1007/s13364-018-0364-2
predator and increasing/decreasing prey handling time (Herrel
et al. 2001; Verwaijen et al. 2002;Herreletal.2006; van der
Meij and Bout 2006; Bulté et al. 2008). Furthermore, closely
related sympatric vertebrates exhibit different craniomandibular
morphologies that facilitate dietary partitioning by allowing each
species to specialize on different prey items (Verwaijen et al.
2002; Mori and Vincent 2008; Santana et al. 2010). These shifts
toward different craniomandibular morphologies, however, are
not only driven by evolutionary processes but may also be driven
by developmental plasticity. A plethora of studies have demon-
strated that differences in dietary consistency can affect the shape
of the skull and dental morphology (Watt and Williams 1951;
Myers et al. 1996;Makietal.2002).
In this study, we examine if the dietary partitioning ob-
served between two sympatric Peromyscus mice are accom-
panied by differences in craniomandibular morphology.
Peromyscus californicus (California mouse) and
Peromyscus truei (pinyon mouse) occur sympatrically in
the Santa Cruz Mountains and can be distinguished primarily
by mean body mass where P. californicus (43.04 g) is larger
than P. t r u e i (26.92 g) (SMURF, unpublished data). Recent
isotopic analyses revealed dietary differences between these
two species (Reid et al. 2013): P. t r u e i (misidentified as
Peromyscus boylii in Reid et al. 2013) primarily specializes
on tanoak acorns (Notholithocarpus densiflorus) during the
winter, spring, and summer monthsand Shreve oak (Quercus
parvula) and California live oak (Quercus agrifolia) acorns
in the fall. In contrast, P. cali fornicus feeds at a higher trophic
level and primarily consumes spiders (Araneae) in addition
to beetles (Coleoptera), crickets (Orthoptera), and some sup-
plementary acorns from N. densiflorus and Q. parvula (Reid
et al. 2013). To better understand the link between dietary
partitioning and craniomandibular variation, we test the hy-
pothesis that P. t r u e i and P. californicus exhibit differences in
craniomandibular size and shape as well as mechanical ad-
vantage of the jaw adductor muscles. We predict that P. t r u e i
will exhibit relatively wider zygomatic arches, more robust
mandibles, and greater mechanical advantage that can facil-
itate relatively stronger biting ability needed to specialize on
hard-shelled acorns.
Materials and methods
Specimens and geometric morphometric superimposition We
quantified differences in the cranium and mandible by analyz-
ing three views of the skull with 2D landmark-based geomet-
ric morphometrics (Rohlf and Slice 1990;Zelditchetal.
2012). We obtained 41 adult P. californicus parasiticus skulls
(16 females, 25 males) and 33 adult P. truei dyselius skulls (15
females, 18 males) from the mammal collection at the
California Academy of Sciences (Supplementary Data 1).
Specimens originated from the Santa Cruz Mountains within
Santa Clara and Santa Cruz counties in California. All speci-
mens were fully mature, determined by the complete eruption
of all cheek teeth (Holmes et al. 2015).
Each specimen was photographed in three views: (1) cra-
nium in ventral view, photographed by orienting the palate
plane parallel to the photographic plane; (2) cranium in lateral
view, photographed by orienting the midsagittal plane parallel
to the photographic plane; and (3) mandible in lateral view,
photographed by orienting the long axis of the dentary parallel
to the photographic plane. Photographs were taken using a
Canon 70D DSLR camera affixed to a Kaiser 205513 RS-10
copy stand kit. Specimens were placed at a distance of 35 cm
away from the camera lens. A ruler with 1 × 1 cm grids was
used to ensure no distortion as well as serve as a scale bar.
Fig. 1 Landmarks (large black circles) and semi-landmarks (small red
circles) used for geometric morphometric analysis of skull shape and size.
Specimen is a male Peromyscus californicus (CAS MAM 12567). The
scale bar represents 1 cm of distance. aVentral cranial view: (1)
anteriormost point of the suture between nasals, (2) and (3) lateralmost
point of the alveolus of the incisor, (4) and (5) lateral tip of the incisor, (6)
and (7) anteriormost point of the incisive foramen, (8) and (9) exterior
ends of the premaxillary-maxillary sutures, (10) and (11) lateralmost ex-
tent of suture between the premaxilla and maxilla, (12) and (13)
anterodorsal tip of zygomatic plate, (14) and (15) posteriormost point of
the incisive foramen, (16) and (17) anteriormost point of the orbit, (18)
and (19) anteriormost point of the molar row, (20) and (21) lateral
paracone of first molar, (22) and (23) contact point between first and
second molars, (24) and (25) contact point between second and third
molars, (26) and (27) posteriormost point of the third molar, (28) and
(29) least post-palatal distance across the palatines, (30) and (31)
anteriormost point of the glenoid fossa, (32) and (33) posterior end of
squamosal root of zygomatic bar, (34) posteriormost extent of palate at
the midline, (35) and (36) suture between basisphenoid and basioccipital
at point of contact with the auditory bulla, (37) and (38) lateral margins of
the foramen ovale, (39) anteriormost point of the foramen magnum along
the midline, (40) posteriormost point of the foramen magnum on the
midline, (41) and (42) lateral margins of the foramen magnum, (43) and
(44) posteriormost margin of the mastoid process. bLateral cranial view:
(1) posteriormost point of the upper incisive alveolus, (2) inferiormost
point of the upper incisive alveolus, (3) interior most point of suture
between nasal and premaxillary, (4) anterior tip of the nasal, (5) curvature
at the limit between the occipital condyle and the occipital bone, (6)
inferior extremity on the boundary between the occipital condyle and
the tympanic bulla, (7) ventral-most point of the interior of the opening
to the tympanic bulla, (8) dorsal-most point of the interior of the opening
to the tympanic bulla, (9) posteriormost point of the molar row, (10)
anteriormost point of the molar row, (11) ventral extent of the suture
between maxilla and premaxilla, (12) anteriormost point of the orbit,
(13) anteriormost point of the glenoid fossa in the zygomatic bar, (14)
posterior end of zygomatic bar. cMandibular view: (1) anteroventral
border of incisive alveolus, (2) upper extreme anterior border of incisor
alveolus, (3) position of greatest inflection of the diastema, (4) Anterior
edge of the alveolus of first molar, (5) intersection between molar crown
and coronoid process in lateral view, (6) tip of the coronoid process, (7)
point of maximum curvature between the coronoid and condylar process,
(8) dorsal margin of the anterior edge of the articular surface of the
condylar process, (9) ventral edge of the articular surface of the condylar
process, (10) point of maximum curvature between condylar and angular
process, (11) tip of the angular process, (12) intersection between man-
dibular body and masseteric crest
b
Mamm Res
We then placed homologous morphological landmarks and
semi-landmarks on the lateral cranial, ventral cranial, and lat-
eral mandibular views. We used 14 landmarks and 26 semi-
landmarks on the lateral cranial view, 44 landmarks and 10
semi-landmarks on the ventral cranium view, and 11 land-
marks and 51 semi-landmarks on the lateral mandibular view
(Fig. 1) based on Maestri et al. (2016). Landmarks were cho-
sen for their potential to be recognized across a species; semi-
landmarks were generated at evenly spaced intervals between
landmarks. All landmarks were digitized using the program
tpsDig-v 2.30 (Rohlf 2005). We then aligned digitized speci-
mens using a generalized Procrustes superimposition (Rohlf
and Slice 1990) in the R package geomorph 3.0.1 (Adams and
Otárola-Castillo 2013) in R 3.2.1 (R Core Team 2017). During
the Procrustes superimposition, semi-landmarks on the curves
were allowed to slide along their tangent vectors until their
positions minimized bending energy (Bookstein 1997;
Zelditch et al. 2012). After superimposition, bilaterally homol-
ogous landmarks on the ventral cranium were reflected across
the midline and averaged using the geomorph function
bilat.symmetry.
Analysis of skull size and shape We first examined if sexual
dimorphism in skull size and shape was significant within
each species. For each species, we determined if the size of
each skull view was significantly different between the sexes
using separate analyses of variance (ANOVAs) on the centroid
size of each configuration of landmarks (the square root of the
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DMAT
OL
MAM
Mamm Res
sum of the squared distances from each landmark to the geo-
metric center of the shape) (Bookstein 1997). Similarly, we
determined if skull shape within each species was significant-
ly different between the sexes using a Procrustes ANOVA
(Goodall 1991; Anderson 2001) with a factorial design on
each of the skull view datasets. For each skull view, we used
shape as the dependent variable, sex as the main factor, and
centroid size as a covariate.
We found no significant sexual dimorphism in size or
shape of any skull view; therefore, we pooled males and fe-
males in our analyses of interspecific differentiation. For each
skull view, we examined differences in skull size and skull
shape using ANOVAs and Procrustes ANOVAs, respectively.
Procrustes ANOVAs were conducted with a factorial design
with shape as the dependent variable, species as the main
factor, and centroid size as a covariate. Procrustes ANOVAs
were performed with the procD.lm function in the R package
geomorph 3.0.1 (Adams and Otárola-Castillo 2013). We also
used a pairwise permutation test with the permudist function
in the R package MORPHO 2.4 (Schlager 2016)toquantify
shape differences (Procrustes distances) between the two spe-
cies and to determine if these differences were significant.
Lastly, we performed separate principal component analyses
on the Procrustes coordinates of each skull view to visualize
the tangent space (form) of the two species.
Mechanical advantage We assessed differences in biting abil-
ity between the two species by modeling the lower jaw as a
lever and calculating mechanical advantage (MA) of the
temporalis and masseter masticatory muscles (e.g., Tanner
et al. 2010; La Croix et al. 2011; Timm-Davis et al. 2015;
Law et al. 2016a). MA describes the proportion of jaw muscle
force transmitted to the bite point; relatively higher MA indi-
cates higher force-modified jaws (Kardong 2014). MA is cal-
culated as the ratio between the in-lever, the distance between
the mandibular condyle and the muscle insertion point, and
the out-lever (OL), the distance from the mandibular condyle
to the tip of the incisor. We used moment arm of temporalis
(MAT), measured from the tip of the coronoid process to the
condyle, and moment arm of masseter (MAM), measured
from the tip of the angular process to the condyle, as our
temporalis and masseter in-lever (moment arm) distances, re-
spectively. The out-lever was measured to the tip of the incisor
(Fig. 1d). ShapiroWilk tests indicated that MA exhibited a
normal distribution. Thus, we performed ANOVAs to deter-
mine whether there were significant sexual differences in MA.
Results
Skull size and shape Skulls of the Peromyscus californicus
were significantly larger than skulls of the P. truei in the ven-
tral cranium (F
1,72
= 155.16, P< 0.001), lateral cranium
(F
1,72
= 4726, P< .001), and mandible (F
1,72
= 4726,
P< 0.001). A principal component analysis of the Procrustes
coordinates revealed form of all three skull views largely sep-
arated out between the two species on PC1 (Fig. 2). Analyses
with both Procrustes ANOVAs and pairwise permutation tests
confirmed significant shape differences for all three skull
views (Table 1; Fig. 3). In the cranium, the P. truei exhibited
relatively longer tooth rows, relatively wider zygomatic
arches, and relatively longer dorsal cranial profiles (Fig. 3a,
b). In the mandible, the P. truei exhibited relatively broader,
more robust masseteric fossa and coronoid process but exhib-
ited a relatively shorter angular process (Fig. 3c).
Procrustes ANOVAs also revealed significant allometry
between shape and size in the crania of both species; however,
these allometric patterns do not significantly differ between
the two species (Table 1). The mandible, in contrast, does not
exhibit significant allometry between mandibular shape and
size (Table 1).
Mechanical advantage Feeding performance was measured as
the MA of the two primary jaw adductor muscles, the
temporalis and masseter muscles. MA of the temporalis did
not differ significantly between the two species (F
1,72
=0.442,
P= 0.508). In contrast, P. truei exhibited significantly greater
MA of the masseter compared to P. californicus (F
1,72
=
21.69, P<0.001).
Discussion
Within the Santa Cruz Mountains, Peromyscus truei and
P. californicus are congeners that coexist in sympatric loca-
tions. Their ability to coexist is hypothesized to be a result of
dietary niche partitioning: P. truei specializes on hard-shelled
acorns, whereas P. californicus primarily feeds on arthropods
such as Araneae, Orthoptera, and Coleoptera (Reid et al.
2013). Consistent with these dietary differences, we found
craniomandibular differences that allow P. truei to be better
suited to process hard-shelled acorns compared to
P. c a l i f o r n i c u s . Specifically, we found that P. truei exhibited
relatively wider zygomatic arches and relatively longer ros-
trum in the cranium and relatively broader mandibular ramus.
These traits serve as attachment sites for the masticatory mus-
cles, particularly the masseter that originates at the zygomatic
arch, spans across the mandibular ramus, and inserts at the
angular process (Turnbull 1970;Cox2008). As the largest
of the masticatory muscles in rodents, the masseter exerts
the strongest force during jaw closure (Turnbull 1970) and
increases bite efficiency at the incisors (Druzinsky 2010).
Therefore, the relatively wider zygomatic arches and broader
mandibular rami found in P. truei suggest relatively larger
masseter muscles and thus relatively greater biting ability than
P. californicus.
Mamm Res
Our finding that P. t r u e i also exhibits greater MA of the
masseter further corroborates these morphological differ-
ences. Higher MA is typically associated with increased
force-modified jaws (Kardong 2014) that are adapted to pro-
cess hard-shelled prey. Unsurprisingly, relatively higher MA
of the masticatory muscles are found in several durophagous
vertebrates such as loggerhead musk turtles (Pfaller et al.
2011), some moray eels (Collar et al. 2014), and southern
sea otters (Law et al. 2016b).
Together, our analyses of the craniomandibular morpholo-
gy and mechanical advantage suggest that, for a given size,
P. t r u e i exhibits relatively greater bite force than
P. californicus. These biomechanical differences in the feed-
ing apparatus often correspond to realized dietary differences
in sympatric species (Verwaijen et al. 2002;MoriandVincent
2008; Santana et al. 2010). Because the force an animal can
generate by biting limits the range of prey items it can con-
sume, greater bite forces strongly correlate with reduced han-
dling times for both prey capture and consumption (Herrel
et al. 2001; van der Meij and Bout 2006; Anderson et al.
2008) and the ability to expand dietary breadth by consuming
larger or more robust food items (Verwaijen et al. 2002;Herrel
et al. 2006; Bulté et al. 2008; Pfaller et al. 2011). In the Santa
Cruz Mountains, a relatively greater bite force allows P. truei
to consume hard-shelled acorns at a greater efficiency than
P. californicus despite its smaller body size. Nevertheless,
the phenomenon of many-to-one mapping of morphology to
function has demonstrated that different morphological traits
Table 1 Results from Procrustes
ANOVAs for species differences
in cranial and mandibular shape
SS MS R
2
F
1, 70
Pvalue
A. Ventral cranium
Species 0.014431 0.014431 0.216963 20.4789 0.001
Centroid size 0.003063 0.0030635 0.046058 4.3474 0.001
Species × size 0.000396 0.0003964 0.00596 0.5626 0.873
Residuals 0.048623 0.0007047
Tot al 0.0 66 5 13
B. Lateral cranium
Species 0.06164 0.06164 0.35627 41.5693 0.001
Centroid size 0.0064 0.0064 0.03699 4.3161 0.005
Species × size 0.001178 0.001178 0.00681 0.7943 0.517
Residuals 0.103797 0.001483
Tot al 0.1 73 0 14
C. Mandible
Species 0.025682 0.0256825 0.143532 12.1203 0.001
Centroid size 0.00385 0.0038498 0.021515 1.8168 0.064
Species × size 0.001073 0.0010731 0.005997 0.5064 0.859
Residuals 0.148327 0.002119
Tot al 0.1 78 9 32
Italicized Pvalues indicate significance (α=0.05)
SS sum of squares, MS means squares
Fig. 2 Principal components plot of skull form variation. Deformation grids display shapes at the ends of the range of variability along PC1 (red=
P. tr u e i , light gray = P. californicus). Shapes of all three skull views are significantly different between the two species (Table 1)
Mamm Res
will not necessarily translate to different functional traits
(Alfaro et al. 2005; Wainwright et al. 2005). Therefore, wheth-
er these differences in craniomandibular morphology between
P. californicus and P. truei results in actual differences in
in vivo bite forces will requires further investigation.
Conclusion
Here, we found that P. truei exhibits craniomandibular mor-
phology (relatively wider zygomatic arches in the cranium
and relatively broader mandibular rami) better suited to pro-
cess hard-shelled acorns along with higher mechanical
advantage of the masseter jaw muscle relative to
P. californius. Although these findings are consistent with
the dietary differences exhibited by P. truei (acorn specialist)
and P. californicus (arthropods), the underlying mechanisms
that led to these morphological differences are not yet clear.
Several confounding factors not analyzed in this present study
may drive these differences including differences in micro-
habitats, sensory adaptations, and/or random evolutionary his-
tory. Future work incorporating specimens across multiple
populations with allopatric and sympatric P. t r u e i and
P. californicus as well as dietary manipulation will elucidate
whether the relationship between craniomandibular and die-
tary differences arose through adaptations toward different
morphological optima or through developmental plasticity in
which different dietary items influenced the development of
the skull and mandible.
Acknowledgements We thank the many mentors, staff, and students of
the University of California, Santa Cruz (UCSC) Small Mammal
Undergraduate Research in the Forest (SMURF) program who have
worked with us and taught us about the natural history of deer mice.
We would like to thank Tina Cheng (UCSC), Karen Holl (UCSC), and
Gage H. Dayton (UCSC) for their support of this study.
Funding Funding for the SMURF program was provided by the UCSC
Department of Ecology and Evolutionary Biology, the Webster Chair
Fund, the Kenneth S. Norris Center for Natural History, and the UC
Natural Reserve System. CJL was funded by a National Science
Foundation Graduate Research Fellowship.
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... Females showed relatively longer moment arms of the ventral fibers of the superficial masseter and anterior deep masseter, which may increase the strength of incisor bite (Casanovas-Vilar & van Dam 2013;Jones & Law 2018). Subsequently, surface area of the vertical ramus (ascending ramus) of the mandible might be increased with respect to the longer mandibular body length in females, although oral (ManneWhitney U ¼ 83.0, P ¼ 0.071) and aboral (ManneWhitney U ¼ 79.5, P ¼ 0.053) heights of the vertical ramus of the mandible statistically did not differ between sexes. ...
... Subsequently, surface area of the vertical ramus (ascending ramus) of the mandible might be increased with respect to the longer mandibular body length in females, although oral (ManneWhitney U ¼ 83.0, P ¼ 0.071) and aboral (ManneWhitney U ¼ 79.5, P ¼ 0.053) heights of the vertical ramus of the mandible statistically did not differ between sexes. Considering only mandible, CVA also indicated that the sexes are highly discriminated by oral and aboral heights of the vertical ramus of the mandible, which may increase the surface area for masticatory muscles (Suzuki et al. 2011;Casanovas-Vilar & van Dam 2013;Jones & Law 2018). Therefore, ascending ramus of the mandible in females of P. leucogenys might have relatively more surface area for muscle attachment. ...
... Casanovas-Vilar & van Dam 2013;Law et al. 2016;Jones & Law 2018). The measurements of the incisor resistance arm (RI) and primary masticatory muscles, such as moment arm of the most dorsal fiber of the temporalis (MT), moment arm of the most ventral fibers of the temporalis (MT2), moment arm of the most dorsally inserting fibers of the superficial masseter (MSM), moment arm of the most ventral fibers of the superficial masseter (MSM2), moment arm of the most anterior fibers of the anterior deep masseter (MADM), were taken following Casanovas-Vilar & van Dam (2013)(Fig. ...
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... Lever arms have been used to provide a reasonable first approximation of MA in a number of previous studies (e.g. Casanovas-Vilar & van Dam, 2013;Renaud et al., 2015;Gomes Rodrigues et al., 2016;Jones & Law, 2018;West & King, 2018), but it should be noted that variations in mandibular morphology can rotate lever arms thus changing moment arms without altering the length of the lever arms. Secondly, the representation of a muscle insertion as a single point is a clear over-simplification as the temporalis, superficial masseter and deep masseter all have large attachment sites on the squirrel mandible (Cox & Jeffery, 2011. ...
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