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Comparative functional analysis of skull morphology of tree-gouging primates.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 120:153–170 (2003)
Comparative Functional Analysis of Skull Morphology of
Tree-Gouging Primates
Christopher J. Vinyard,2* Christine E. Wall,1 Susan H. Williams,1 and William L. Hylander1,2
1
Department of Biological Anthropology and Anatomy, Duke University Medical Center,
Durham, North Carolina 27710
2
Duke University Primate Center, Durham, North Carolina 27710
KEY WORDS
tree gouging; skull functional morphology; gape; forces; load resistance
ABSTRACT
Many primates habitually feed on tree
exudates such as gums and saps. Among these exudate
feeders, Cebuella pygmaea, Callithrix spp., Phaner furcifer, and most likely Euoticus elegantulus elicit exudate
flow by biting into trees with their anterior dentition. We
define this behavior as gouging. Beyond the recent publication by Dumont ([1997] Am J Phys Anthropol 102:187–
202), there have been few attempts to address whether
any aspect of skull form in gouging primates relates to this
specialized feeding behavior. However, many researchers
have proposed that tree gouging results in larger bite
force, larger internal skull loads, and larger jaw gapes in
comparison to other chewing and biting behaviors. If true,
then we might expect primate gougers to exhibit skull
modifications that provide increased abilities to produce
bite forces at the incisors, withstand loads in the skull,
and/or generate large gapes for gouging.
We develop 13 morphological predictions based on the
expectation that gouging involves relatively large jaw forces
and/or jaw gapes. We compare skull shapes for P. furcifer to
five cheirogaleid taxa, E. elegantulus to six galagid species,
and C. jacchus to two tamarin species, so as to assess
whether gouging primates exhibit these predicted morphological shapes. Our results show little morphological evidence for increased force-production or load-resistance abilities in the skulls of these gouging primates. Conversely,
these gougers tend to have skull shapes that are advantageous for creating large gapes. For example, all three gouging species have significantly lower condylar heights relative
to the toothrow at a given mandibular length in comparison
with closely related, nongouging taxa. Lowering the height
of the condyle relative to the mandibular toothrow should
reduce the stretching of the masseters and medial pterygoids
during jaw opening, as well as position the mandibular incisors more anteriorly at wide jaw gapes. In other words, the
lower incisors will follow a more vertical trajectory during
both jaw opening and closing.
We predict, based on these findings, that tree-gouging
primates do not generate unusually large forces, but that
they do use relatively large gapes during gouging. Of
course, in vivo data on jaw forces and jaw gapes are
required to reliably assess skull functions during gouging.
Am J Phys Anthropol 120:153–170, 2003.
Tree exudates provide an essential food source for
many primates (Kinzey et al., 1975; Charles-Dominique, 1977; Charles-Dominique and Petter, 1980;
Sussman and Kinzey, 1984; Nash, 1986; Garber,
1992). Field researchers have observed exudate feeding or gummivory in at least 37 primate species, including representative taxa for most primate superfamilies (see Coimbra-Filho and Mittermeier, 1977;
Garber, 1984; Nash, 1986 and references therein).1
Many of these species possess suites of morphological
features that have been hypothesized to be functionally linked to exudate feeding, such as small body size,
robust lower incisors, caniniform upper premolars,
claw-like tegulae, camouflaged pelage, and/or expanded stomachs or large intestines (Kinzey et al.,
1975; Petter et al., 1977; Hershkovitz, 1977; Rosenberger, 1978; Charles-Dominique and Petter, 1980;
Chivers and Hladik, 1980, 1984; Coimbra-Filho et al.,
1980; Garber, 1980; Martin, 1990; Hamrick, 1998).
A limited number of field observations suggest that
some of these gummivorous primate species actively
elicit tree exudate flow by mechanically damaging
trees with their anterior teeth. We define this type of
biting behavior as gouging (Stevenson and Rylands,
©
2003 WILEY-LISS, INC.
©
2003 Wiley-Liss, Inc.
1
Nash (1986) discusses the potential differences in the definitions of
exudate feeding vs. gummivory. We use these terms synonymously to
include the relevant literature that applies either term to describe
this feeding behavior.
Grant sponsor: Sigma-Xi; Grant sponsor: Boise Fund; Grant sponsor: AMNH; Grant sponsor: NSF; grant numbers SBR-9701425; Grant
sponsor: L.S.B. Leakey Foundation.
*Correspondence to: Christopher J. Vinyard, Department of Biological Anthropology and Anatomy, Box 3170, Duke University Medical
Center, Durham, NC 27710. E-mail: cvinyard@acpub.duke.edu
Received 13 February 2001; accepted 16 April 2002.
DOI 10.1002/ajpa.10129
Published online in Wiley InterScience (www.interscience.wiley.
com).
154
C.J. VINYARD ET AL.
1988). Several of these gouging primates have elongate, labio-lingually thick, or otherwise modified anterior tooth crowns thought to be related functionally to
gouging (Martin, 1972, 1979, 1990; Charles-Dominique, 1977; Coimbra-Filho and Mittermeier, 1977; Szalay and Seligsohn, 1977; Rosenberger, 1978; Muskin,
1984; Eaglen, 1986; Natori and Shigehara, 1992).
Compared to the information on dental functional
morphology, primatologists know far less about how
the mechanical demands of gouging affect skull form
in these primates (Dumont, 1997).
Dumont (1997) examined skull shapes in several
tree-gouging primates and marsupials. Species of
primates, bats, and marsupials were compared together in a discriminant function analysis to determine if morphological adaptations to tree gouging
could be recognized in the skull. The phylogenetic
breadth of species included in the analysis was offered as an attempt to “highlight anatomical features that are correlated with dietary habit and to
minimize emphasis on features that characterize
closely related species” (Dumont, 1997, p. 188).
We take a different view of this approach to discerning form-function relationships in specific taxa. We
argue that lumping such phylogenetically diverse species in a single analysis makes it difficult, if not unlikely, to determine what component of variation in
skull form among these species is related to the mechanical demands of tree gouging vs. skull variation
linked to other evolutionary events that occurred during the largely separate phylogenetic histories of these
various species (Felsenstein, 1985; Huey and Bennett,
1986, 1990; Bennett and Huey, 1990; Brooks and
McLennan, 1991; Garland and Adolph, 1994; Harvey
and Pagel, 1991; Miles and Dunham, 1993). Here we
utilize an alternative method. We carry out multiple,
pairwise morphometric comparisons of primate tree
gougers to closely related species that do not gouge
trees in order to assess differences in skull form that
may be functionally related to gouging (Harvey, 1991;
Moller and Birkhead, 1992; Purvis and Bronham,
1997; Maddison, 2000). This more phylogenetically restricted approach does not eliminate all confounding
factors (e.g., size-correlated changes in shape), but it
does reduce the complications created by comparing
diverse species with markedly different phylogenetic
histories.
PRIMATE TREE GOUGERS
The behavioral evidence for habitual tree gouging
associated with exudate feeding is limited for most
primates, with the exception of several marmosets.
Based on available field reports, we consider Callithrix spp., Cebuella pygmaea,2 Phaner furcifer, and
2
We did not include Cebuella pygmaea in this study because not
enough individuals could be measured, and there is no adequate,
nongouging sister species of approximately similar body size for comparison.
Euoticus elegantulus to be habitual tree-gouging
species. We base this decision on the combination of
three criteria. First, these species have been observed using their anterior teeth to either elicit exudate flow or extract exudates from trees (Petter
et al., 1971, 1977; Charles-Dominique, 1974, 1977;
Kinzey et al., 1975; Coimbra-Filho and Mittermeier,
1976, 1977; Ramirez et al., 1977; Charles-Dominique and Petter, 1980; Lacher et al., 1981, 1984;
Rylands, 1981, 1984; Maier et al., 1982; Soini, 1982;
Sussman and Kinzey, 1984; Stevenson and Rylands,
1988). Second, field observations and/or data from
stomach contents show that exudates form a large
percentage of the diet for these species (Petter et al.,
1971, 1977; Charles-Dominique, 1974, 1977; Pariente, 1975; Ramirez et al., 1977; Szalay and Seligsohn, 1977; Charles-Dominique and Bearder, 1979;
Hladik, 1979; Charles-Dominique and Petter, 1980;
Hladik et al., 1979; Lacher et al., 1981; Maier et al.,
1982; Fonseca and Lacher, 1984; Sussman and Kinzey, 1984). Third, each of these species exhibits derived dental morphologies that are arguably functionally linked to tree gouging (Martin, 1972, 1979;
Petter et al., 1971, 1977; Coimbra-Filho and Mittermeier, 1976, 1977; Charles-Dominique, 1977; Szalay
and Seligsohn, 1977; Rosenberger, 1978, 1992;
Charles-Dominique and Petter, 1980; Muskin, 1984;
Sussman and Kinzey, 1984; Eaglen, 1986; Nash,
1986; Stevenson and Rylands, 1988; Garber, 1992;
Natori and Shigehara, 1992; Ferrari, 1993). Future
field observations may add to this list of habitual
tree gougers.
MORPHOLOGICAL PREDICTIONS LINKED
TO TREE GOUGING
Several researchers suggest that tree gouging
among specific primates produces large forces at the
jaw or results in large jaw gapes relative to other
behaviors involving the oral apparatus (Szalay and
Seligsohn, 1977; Szalay and Delson, 1979; Dumont,
1997; Williams and Wall, 1999; Spencer, 1999; Vinyard, 1999; Williams et al., 2000). We want to be
clear, however, that presently we lack sufficient in
vivo data demonstrating that jaw forces and/or
gapes are relatively large during gouging (for preliminary in vivo data, see Vinyard et al., 2001). Our
goal in this study was to determine if there are
changes in skull form in gouging primates that can
be functionally related to the hypothesized large jaw
forces and/or jaw gapes during gouging. We make
two assumptions in our morphological comparisons:
1) that we can reasonably infer certain aspects of
jaw forces, skull loads, and jaw gapes during gouging from in vivo and comparative data on primate
incising and biting along their anterior teeth, and 2)
that existing skull forms in gouging primates represent functional and/or evolutionary adaptive responses to these supposed increased functional demands. If a tree-gouging species exhibits a predicted
morphology in all pairwise comparisons with non-
SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES
gouging species in its family or subfamily, then correlational support is offered suggesting that a particular skull form is functionally linked to gouging in
that species.
Predictions related to large jaw
forces during gouging
Several researchers suggest that tree gouging produces large jaw forces relative to other activities
involving the oral apparatus (Szalay and Seligsohn,
1977; Szalay and Delson, 1979; Dumont, 1997; Williams and Wall, 1999; Spencer, 1999; Vinyard,
1999). We apply in vivo observations of skull loadings and jaw muscle-activity patterns during anterior tooth use (Hylander, 1979a, 1984; Hylander and
Johnson, 1985), comparative studies of primate
skulls (Hylander, 1979b, 1988; Ravosa, 1991, 1996a;
Daegling, 1992; Cole, 1992; Ravosa and Hylander,
1994), and theoretical biomechanical expectations
(e.g., Gysi, 1921; Maynard Smith and Savage, 1959;
Turnbull, 1970; Hylander, 1975; Smith, 1978) to
infer four predicted morphologies (predictions 1– 4)
that would provide increased resistance to the internal loads created by these large gouging forces. Predictions 5–7 are taken from the findings made by
Dumont (1997). Prediction 5 suggests a morphological response that would offer increased load resistance. Prediction 6 relates to increasing mechanical
advantage for gouging, while prediction 7 pertains
to producing larger jaw-muscle forces. Prediction 8
also focuses on increasing mechanical advantage for
gouging. All eight predictions state the expected
morphology if gouging routinely involves relatively
large external forces acting on the skull. All predictions are stated relative to the nongouging condition
for the respective family or subfamily.
Prediction 1: tree gougers have deeper mandibular corpora. In vivo data in macaques indicate
that both mandibular corpora are bent in a parasagittal plane during incision and biting along the anterior teeth (Hylander, 1979a,b, 1988). Increasing
the vertical depth of the corpus is a more effective
way of providing greater resistance to parasagittal
bending moments than increasing the thickness of
the corpus (Hylander, 1979a,b, 1988; Ravosa, 1991,
1996a; Daegling, 1992; Ravosa and Hylander, 1994).
Prediction 2: tree gougers have thicker (or
wider) mandibular corpora. Both mandibular
corpora are also twisted about their long axes during
incision and anterior tooth biting in macaques (Hylander, 1979a,b, 1988). Generally, the most effective
solution for resisting this torsion is to increase the
mediolateral (ML) width of the corpus, rather than
increasing the vertical depth of the corpus (Hylander, 1979a,b, 1988; Ravosa, 1991, 1996a; Daegling, 1992; Ravosa and Hylander, 1994).
155
Prediction 3: tree gougers have vertically elongated symphyses. In vivo data in macaques show
that the symphysis is primarily bent in a frontal
plane during incision and anterior tooth biting due
to the twisting of the mandibular corpora about
their long axes (Hylander, 1984, 1985, 1988). This
vertical bending results in compression along the
alveolar region and tension along the basal portion
of the symphysis. Setting aside the possibility of
fusing the symphysis, increasing the vertical or dorsoventral (DV) length of the symphysis is one of two
effective solutions for resisting this bending (Hylander, 1984, 1985, 1988; Daegling, 1992; Ravosa
and Hylander, 1994; Ravosa and Simons, 1994). The
other solution is to create a simian shelf (Hylander
1984, 1985).
Prediction 4: tree gougers have larger condyle
articular surface areas. Macaque mandibular
condyles are loaded in compression during incision
and biting at the anterior teeth (Hylander, 1979c;
Hylander and Bays, 1979). Presumably, increasing
condylar articular area offers a larger surface for
resisting the potentially higher condylar reaction
forces during gouging (Hylander, 1979b; Smith
et al., 1983; Herring, 1985; Bouvier, 1986a,b; Wall,
1999).
Prediction 5: tree gougers have wider crania in
the temporal fossa region. Dumont (1997) found
that tree-gouging primates have relatively wider
crania between the temporal fossae. Increasing the
relative width of the cranium in this region is argued to buttress the junction between the neurocranium and viscerocranium, and hence provide
greater resistance to loads during tree gouging (Dumont, 1997).
Prediction 6: tree gougers have shorter mandibles. Dumont (1997) found that tree gougers have
relatively short mandibles. She argued that all other
factors being equal, relatively shorter mandibles increase the mechanical advantage of the jaw muscles
during gouging at the anterior dentition.
Prediction 7: tree gougers have condyles elevated higher above the mandibular occlusal
plane. Dumont (1997) found that tree gougers
have relatively higher condyles above the occlusal
plane. She rightly argued that these higher condyles
facilitate a relative increase in size of the masseter
and medial pterygoid muscles, and relatively larger
muscles provide greater jaw-adductor force for tree
gouging (Dumont, 1997).
Prediction 8: tree gougers have longer masseter
moment arms. All other factors being equal, increasing the length of the masseter moment arm
increases the mechanical advantage of the masseter
during gouging at the anterior teeth.
156
C.J. VINYARD ET AL.
TABLE 1. Primate sample used in comparing
skull morphologies
Predictions related to large jaw gapes
during gouging
Preliminary observations in a laboratory setting
suggest that Callithrix jacchus uses relatively larger
maximum gapes, i.e., more widely opened jaws, during gouging vs. maximum gapes during insect chewing (Williams et al., 2000; Vinyard et al., 2001, and
unpublished data). These larger gapes may be beneficial both for aligning the incisal cutting edge for
penetrating the tree substrate and increasing the
potential jaw-closing trajectory for removing isolated tree pieces. We hypothesize that tree-gouging
primates routinely use larger maximum gapes during gouging than during other biting, chewing, and
display activities. Below, predictions 9 –13 state
what morphology would be associated with large
maximum gapes. All predictions are relative to the
nongouging condition in the family or subfamily.
Prediction 9: tree gougers have longer mandibles. Gapes are created primarily by rotating the
mandible about the rest of the skull. Gape typically
is measured as the distance between the maxillary
and mandibular central incisors at any point during
this rotation. For a given degree of mandibular rotation, longer mandibles produce larger gapes. The
prediction that gougers have longer mandibles is the
opposite of prediction 6 taken from Dumont (1997).
Prediction 10: tree gougers have lower condyles
relative to the mandibular occlusal plane.
The extent that a jaw muscle can be stretched is an
important factor affecting the maximum gape of an
animal. Herring and Herring (1974) provided a geometric model showing that increasing the included
angle from a jaw muscle’s origin and insertion to the
temporomandibular joint (TMJ) reduces the stretching in this muscle for a given gape. Lowering condyle
height relative to the mandibular occlusal plane effectively increases this angle for the masseter and
medial pterygoid. Thus, relatively lower condyles reduce stretching, and facilitate larger gapes during
gouging. The prediction of lower condyle height is the
opposite of prediction 7 taken from Dumont (1997).
Prediction 11: tree gougers have higher masseter origin-insertion ratios. The model by Herring and Herring (1974) also shows that altering the
ratio of a jaw muscle’s origin to insertion length,
both measured to the TMJ, changes the amount this
muscle is stretched for a given gape. A muscle is
stretched less, making larger gapes possible, as this
origin-insertion ratio departs in either direction
from a value of 1.0 (Herring and Herring, 1974;
Herring, 1975). All primates in this study have a
masseter origin-insertion ratio greater than 1.0.
Therefore, we predict that gougers have higher origin-insertion ratios to facilitate larger gapes.
Primate species1
Cheirogaleidae
Phaner furcifer
Cheirogaleus major
Cheirogaleus medium
Microcebus murinus
Microcebus rufus
Mirza coquereli
Galagidae
Euoticus elegantulus
Galago gallarum
Galago moholi
Galago senegalensis
Galagoides alleni
Galagoides demidoff
Galagoides zanzibaricus
Callitrichinae
Callithrix jacchus
Leontopithecus rosalia
Saguinus fuscicollis
Sample
size (n)
Diet2
Body
mass (g)3
12
13
13
11
12
9
Go/F
F/I
F/I
I/F/G
F/I
F/I/G
460
400
283
61
48
315
25
9
14
33
12
21
10
Go/F/I
F/I
1/F/G
I/F
F/I
I/F/G
I/F
274
200
180
213
273
62
143
26
10
26
Go/I
F/I/G
I/G
321
609
351
1
Extant taxonomy from Fleagle (1999).
Dietary data are from Bearder and Martin (1980), Nash (1986),
Harcourt (1990), Mittermeier et al. (1994), Kinzey (1997), Fleagle
(1999), and references therein. F, frugivory; G, gummivory; Go,
tree-gouging gummivory; I, insectivory; L, folivory.
3
Body mass estimates are in grams (g). Body mass data are the
average of male and female body mass estimates from Smith and
Jungers (1997) and Fleagle (1999).
2
Prediction 12: tree gougers have anteroposteriorly elongated mandibular condyles. The primate mandible rotates on the articular surface of
the condyle about an approximate ML axis during
jaw opening and closing (Hiiemae and Kay, 1973;
Kay and Hiiemae, 1974a,b; Hylander et al., 1987;
Wall, 1999). Increasing the relative AP length of the
condyle (an estimate of the condyle’s radius of curvature) increases the range of rotational excursion
of the mandible and hence facilitates larger gapes
(cf. Currey, 1984; Ruff, 1988; Hamrick, 1996).
Prediction 13: tree gougers have anteroposteriorly elongated temporal articular surfaces.
The primate condyle translates anteriorly on the
articular surface of the temporal bone (i.e., the
glenoid fossa, articular eminence, and preglenoid
plane) during jaw opening. The extents of condylar
rotation and translation are correlated with the
magnitude of a gape during jaw opening (Hiiemae
and Kay, 1973; Kay and Hiiemae, 1974a,b; Hylander
et al., 1987; Wall, 1999). It is predicted that increasing the AP length of the articular surface of the
temporal bone facilitates greater condylar translation and hence allows larger gapes.
MATERIALS AND METHODS
Sample
We measured a sample of 256 skulls from 3 gouging and 13 nongouging primates species (Table 1).
We compared each of the three species thought to
gouge trees with the nongouging species from the
157
SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES
TABLE 2. Measurements and variables used to compare skull morphologies in gouging vs. nongouging primates1
Definition2
Skull measurements and variables
Corpus depth (CorpDep)
Corpus width (CorpWid)
Symphysis length (SymLng)
Condyle length (CondL)
Condyle width (CondW)
Bizygomatic breadth (ZYB)
Temporal fossa width (TempWid)
Mandible length (MandL)
Condyle height (ConMandHt)
AP mandible length (APMandL)
Masseter origin length (MassOr)
Masseter insertion length (MassIn)3
Temporal articular surface length (TempL)
Cranial length (CranLng)
Facial length (NPH)
Posterior tooth row length (PTLen)
Symphysis width (SymWid)
Maxillary arch width (BiPalBrd)
Biglenoid breadth (BiGlenBrd)
M1 width (UmolWid)
Condyle area (CondArea)
Minimum cranial width (MCW)
Masseter origin-insertion Ratio
Skull geometric mean (GM)
Superoinferior (SI) distance of mandibular corpus at M1
Mediolateral (ML) distance of mandibular corpus at M1
Distance from incisor alveolus to inferior aspect of symphysis
Anteroposterior (AP) length of condylar articular surface
ML width of condylar articular surface
Transverse distance across zygomatic arches
Maximum ML width of temporal fossa
Infradentale to posterior extent of condyle
Perpendicular distance from top of condyle to mandibular occlusal
plane
Distance from infradentale to posterior margin of ramus, parallel to
occlusal plane
Distance from masseter tubercle to postglenoid process
Distance from condyle to anteroinferior extent of masseter attachment
on mandible
AP length of temporomandibular joint articular surface on temporal
bone
Distance from prosthion to episthocranion
Distance from nasion to prosthion
Mesiodistal length of maxillary premolars and molars
Labiolingual length of symphysis perpendicular to SymLng
Distance between buccal grooves of left and right M1
Transverse distance between lateral extent of glenoid fossae
Maximum buccolingual width of upper first molar
1/2(CondL) * 1/2(CondW) * ␲
ZYB ⫺ (2 * TempWid)
Massor/MassIn
(MandL * CorpDep * CorpBrd * SymWid * SymLng * UmolWid * NPH
* CranLng * BiPalBrd * BiGlenBrd * PTLen)1/11
Prediction
number
1
2
3
4, 12
4
5
5
6
7, 10
9
11
8, 11
13
4
5
11
1
Each measurement and variable is briefly defined and referenced for its relevant prediction(s). See Vinyard (1999) for further
information.
Linear dimensions are in mm and area dimensions are in mm2.
3
We used this measurement as an estimate of masseter moment arm length for testing prediction 8 (Jablonski 1993).
2
same subfamily or family (Table 1). Whenever possible, we included near-equal numbers of males and
females for each species. We combined males and
females from each species for analysis, because we
have no reason to believe there are sex-specific differences in gouging behavior.
Skull measurements and biomechanical
shape variables
We took 20 measurements on each skull (Table 2).
We measured these dimensions to the nearest 0.01
mm, using either digital calipers (Fowler UltraCal
III) on actual skulls or video images of skulls imported into SigmaScan Pro 4.0 software (SPSS, Inc.).
Collection of video images followed the procedures
outlined by Spencer and Spencer (1995).
We assessed the predicted morphological differences between tree-gouging and nongouging species
using biomechanical shape variables. Shape variables provide a scale-free way of examining variation across a size range by considering differences in
form as a ratio of the dimension of interest to a
second-criterion variable (Mosimann, 1970; Darroch
and Mosimann, 1985; Falsetti et al., 1993; Jungers
et al., 1995). We calculated shape variables as the
ratio of the variable of interest to mandible length
(MandL) for most comparisons.3 We used mandible
length as a biomechanical standard because we are
interested in the functional consequences of skull
form for gouging. Mandible length is both an estimate of the load arm during biting at the anterior
teeth (e.g., Hylander, 1979a,b, 1985, 1988; Bouvier,
1986a; Daegling, 1989) and an important component
of linear gape at the incisors (e.g., Lucas, 1981, 1982;
Smith, 1984).4 By using mandible length as a biomechanical standard, we were able to compare
gouger and nongouger skulls while holding constant
relevant mechanical factors thought to be significant
in influencing skull loading and jaw gape. However,
by using this biomechanical standard, we are not
3
The square root of condyle area (CondArea) was used in calculating
the shape variable for this dimension. A shape variable was not
created for the masseter origin-insertion ratio because it is already
dimensionless.
4
Other biomechanical standards have been used to study the mechanical abilities of the mandibular corpus for resisting chewing and
incisal loads. For example, Hylander (1979b, 1988) analyzed the ability of the mandibular corpus at the molar region to counter parasagittal bending by scaling corpus depth relative to the moment arm
acting along this portion of the corpus. We repeated our analyses
using an estimate of this moment arm length. As both results gave the
same interpretation, we only report those using mandible length as a
biomechanical standard.
158
C.J. VINYARD ET AL.
conducting an allometric analysis relative to a general skull size estimate. We may not be “controlling
for size,” as is often attempted with allometric size
corrections, nor are we necessarily able to examine
size-correlated changes in shape (e.g., Smith, 1993;
Jungers et al., 1995). We used a geometric mean of
11 skull measurements (GM) as a skull size estimate
when comparing mandible length and AP mandible
length in predictions 6 and 9, respectively (Table 2).5
Statistical analyses
We conducted all possible pairwise comparisons
per variable between a gouging vs. nongouging species for a family or subfamily. Given the variation in
diet and body mass among the species in each group
(Table 1), we argue that the multiple pairwise comparisons offer a more thorough assessment of the
predicted morphologies in gouging primates by varying these other factors that also potentially affect
skull form. Performing multiple comparisons per
gouging species also lessens statistical problems encountered when only comparing two species (Garland and Adolph, 1994).
We used one-tailed, Mann-Whitney U-tests to assess the predicted differences in skull shapes between individuals of gouging vs. nongouging species.
The P-value for determining statistical significance
was calculated using the large sample equations in
Siegal and Castellan (1988). When a biomechanical
shape variable for a gouging species was significantly different in the predicted direction for all
pairwise comparisons with nongouging species in its
family or subfamily, then correlational support was
offered, suggesting that a particular skull shape is
functionally linked to gouging in that species. If the
one-tailed Mann-Whitney U-test did not show the
predicted significant difference for a variable in a
pairwise comparison, then we performed a twotailed Mann-Whitney U-test to look for an overall
difference in that variable between the two species
(Zar, 1999). A significant difference in the two-tailed
test indicates that the variable is significantly different between the two species in the direction opposite from the prediction.
We assessed 13 morphological predictions for each
pairwise species comparison. Because of the multiple statistical comparisons for each pair of species,
the sequential Bonferroni technique was applied to
set a pairwise significance level of ␣ ⫽ 0.05 for all
statistical comparisons involving a gouging and
nongouging species (Rice, 1989).
5
Across a sample of 97 primate species means, mandible length is
highly correlated (0.996) with the geometric mean used here. Mandible length scales nearly isometrically with this geometric mean (LS
slope ⫽ 0.98 ⫾ 0.02).
RESULTS
Morphological predictions related to large
gouging forces in the skull
Tree gouging species infrequently exhibit the morphologies predicted to be linked to large jaw forces
during gouging (Table 3). With only one exception
(see below), no predicted morphology is always observed in a gouging species relative to all other
nongouging species in the same family or subfamily
(Table 3). Further, there are few pairwise species
comparisons where gouging species showed a significant shape difference in the predicted direction.
Phaner furcifer does not show the skull shapes
predicted to be linked to relatively large jaw forces
in most pairwise comparisons with nongouging cheirogaleids (Table 3a). Although P. furcifer possesses
more robust mandibular corpora, symphyses, and
condyles relative to Microcebus rufus, and to a lesser
extent to M. murinus and Mirza coquereli (Table 3a),
this is not the case for comparisons with Cheirogaleus major or C. medius.
Euoticus elegantulus exhibits the largest number
of predicted shape differences relative to nongouging
galagids (Table 3b). E. elegantulus often has significantly deeper and thicker mandibular corpora,
longer symphyses, and larger condyles for a given
size in comparison to nongouging galagids (Table
3b). However, no predicted shape variable is significantly larger in E. elegantulus in all pairwise comparisons with nongouging galagids. Contrary to prediction 5, minimum cranial width shape is either not
different or is actually significantly narrower in E.
elegantulus relative to other galagids (Table 3b).
Mandible length also is not significantly different in
E. elegantulus vs. these other galagids (Table 3b). E.
elegantulus has a significantly longer relative masseter moment arm length than G. alleni or G. demidoff, but is not statistically different from the remaining galagids. While E. elegantulus appears to have a
relatively robust jaw compared to most galagids,
these results do not meet our strict criteria for linking skull form and gouging forces.
Most skull shapes in Callithrix jacchus are either
similar to nongouging callitrichids or differed significantly from them in the direction opposite from the
prediction (Table 3c). Only minimum cranial width
shape is significantly wider in C. jacchus vs. all
other callitrichids (Table 3c). This predicted shape
difference is the only one in this study that meets
our criteria for linking skull form and gouging
forces.
Morphological predictions related to large
jaw gapes during gouging
Tree gouging primates exhibit several of the shape
differences predicted to facilitate larger gapes in
comparisons with nongouging species from the same
family or subfamily (Table 3). For example, each of
the three gouging species always has significantly
159
SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES
TABLE 3. Results of pairwise species comparisons of skull shapes for (a) Phaner furcifer vs. other cheirogaleids, (b) Euoticus
elegantulus vs. other galagids, and (c) Callithrix jacchus vs. other callitrichids
a. P. furcifer vs. cheirogaleids
Shape variable1
Cheirogaleus
major2
Cheirogaleus
medius
Microcebus
murinus
Microcebus
rufus
Mirza
coquereli
1. M1 depth (Pf ⬎)
2. M1 width (Pf ⬎)
3. Symphysis length (Pf ⬎)
4. Condyle area (Pf ⬎)
5. Minimum cranial width (Pf ⬎)
6. Mandible length (Pf⬍)
7. Condyle height (Pf ⬎)
8. Masseter moment arm (Pf ⬎)
9. AP mandible length (Pf ⬎)
10. Condyle height (Pf⬍)
11. Masseter origin-insertion ratio (Pf ⬎)
12. Condyle length (Pf ⬎)
13. Temporal articular surface length (Pf ⬎)
Ns/0.009
Ns/Ns
0.01/Ns
Ns/Ns
0.01/Ns
Ns/Ns
Ns/⫺
Ns/Ns
Ns/Ns
0.0006/⫺
0.004/⫺
0.002/⫺
0.007/Ns
Ns/0.001
Ns/Ns
0.02/Ns
0.01/Ns
Ns/Ns
Ns/Ns
Ns/⫺
0.002/⫺
Ns/Ns
0.003/⫺
Ns/0.0006
0.001/⫺
Ns/Ns
Ns/Ns
Ns/Ns
0.006/Ns
0.002/⫺
Ns/Ns
Ns/Ns
Ns/⫺
Ns/Ns
Ns/Ns
0.0001/⫺
Ns/Ns
0.0004/⫺
0.001/⫺
0.005/⫺
0.005/⫺
0.0001/⫺
0.0007/⫺
Ns/Ns
0.04/Ns
Ns/⫺
0.005/⫺
Ns/Ns
0.00008/⫺
Ns/Ns
0.00004/⫺
0.007/⫺
Ns/Ns
Ns/Ns
0.009/Ns
0.0007/⫺
Ns/Ns
Ns/Ns
Ns/⫺
Ns/Ns
Ns/Ns
0.0005/⫺
Ns/Ns
0.0002/⫺
0.002/⫺
b. E. elegantulus vs. galagids
Shape variable
Galagoides
alleni
Galago
moholi
Galago
senegalensis
Galagoides
zanzibaricus
Galagoides
demidoff
Galagoides
gallarum
1. M1 depth (Ee⬎)
2. M1 width (Ee⬎)
3. Symphysis length (Ee⬎)
4. Condyle area (Ee⬎)
5. Minimum cranial width (Ee⬎)
6. Mandible length (Ee⬍)
7. Condyle height (Ee⬎)
8. Masseter moment arm (Ee⬎)
9. AP mandible length (Ee⬎)
10. Condyle height (Ee⬍)
11. Masseter origin-insertion ratio (Ee⬎)
12. Condyle length (Ee⬎)
13. Temporal articular surface length (Ee⬎)
0.00005/⫺
0.02/Ns
0.000009/⫺
0.0001/⫺
0.02/Ns
Ns/Ns
Ns/⫺
0.005/⫺
Ns/0.01
0.000003/⫺
0.0007/⫺
0.004/⫺
0.00001/⫺
0.001/⫺
0.001/⫺
0.00002/⫺
0.0005/⫺
Ns/0.00005
Ns/0.02
Ns/⫺
Ns/Ns
0.02/Ns
0.000001/⫺
Ns/Ns
0.002/⫺
0.00004/⫺
0.00003/⫺
0.02/Ns
0.000001/⫺
0.02/Ns
Ns/0.00008
Ns/0.01
Ns/⫺
Ns/Ns
0.03/Ns
0.000001/⫺
Ns/Ns
Ns/Ns
0.00001/⫺
0.000006/⫺
0.01/Ns
0.00001/⫺
0.00009/⫺
Ns/Ns
Ns/Ns
Ns/⫺
0.03/Ns
Ns/0.02
0.000003/⫺
Ns/Ns
0.00005/⫺
0.00003/⫺
0.000002/⫺
0.00004/⫺
0.008/Ns
Ns/Ns
Ns/0.003
Ns/Ns
Ns/⫺
0.001/⫺
Ns/Ns
0.000001/⫺
Ns/Ns
0.05/Ns
0.000001/⫺
0.05/Ns
Ns/Ns
0.006/Ns
Ns/Ns
Ns/0.02
Ns/0.006
Ns/⫺
Ns/Ns
0.01/Ns
0.0006/⫺
0.02/Ns
Ns/Ns
0.00002/⫺
c. C. jacchus vs. callitrichids
Shape variable
1. M1 depth (Cj⬎)
2. M1 width (Cj⬎)
3. Symphysis length (Cj⬎)
4. Condyle area (Cj⬎)
5. Minimum cranial width (Cj⬎)
6. Mandible length (Cj⬍)
7. Condyle height (Cj⬎)
8. Masseter moment arm (Cj⬎)
9. AP mandible length (Cj⬎)
10. Condyle height (Cj⬍)
11. Masseter origin-insertion ratio (Cj⬎)
12. Condyle length (Cj⬎)
13. Temporal articular surface length (Cj⬎)
Leontopithecus rosalia
Saguinus fuscicollis
Ns/0.02
Ns/0.0001
Ns/Ns
Ns/Ns
0.0001/⫺
Ns/0.006
Ns/⫺
Ns/0.04
0.004/⫺
0.000002/⫺
0.00001/⫺
0.01/Ns
0.000002/⫺
Ns/Ns
Ns/0.003
Ns/0.008
Ns/Ns
0.0001/⫺
0.04/Ns
Ns/⫺
Ns/Ns
0.02/Ns
0.000008/⫺
0.0005/⫺
0.00003/⫺
0.000001/⫺
1
We list shape variables predicted to differ in gouging vs. nongouging species at left. We indicate directionality of predicted difference
by specifying whether gouging species should have a relatively larger (e.g., Pf⬎) or relatively smaller (e.g., Pf⬍) shape.
2
We use Mann-Whitney U-tests for all pairwise shape comparisons, and report P-values from these comparisons as described below.
First entry is the P-value from a one-tailed Mann-Whitney U-test of predicted difference in shape between gouging vs. nongouging
species in that pairwise comparison. Second entry gives the result of a two-tailed Mann-Whitney Whitney U-test for a difference in
shape between the two species. Two-tailed tests were only performed when the one-tailed test resulted in no statistical difference in
shape between two species. A significant result in two-tailed test indicates a difference in shape between two species that is opposite
to the predicted pattern. Bold P-values signify a significant difference in shape (␣ ⫽ 0.05) after accounting for multiple shape
comparisons between those two species, using an adjusted Bonferroni method. P-values that are not bold indicate a P-value less than
0.05, but not significant after accounting for multiple shape comparisons between those two species. Ns indicates a P-value larger than
0.05 and represents no statistical difference in shape between those two taxa.
lower condyle height shapes relative to nongouging
species (Fig. 1).
P. furcifer possesses significantly lower condyle
heights and anteroposterior (AP) elongated condyles
for a given size relative to all nongouging cheirogaleids in this study (Table 3a). Relative AP temporal
articular length in P. furcifer is significantly longer
than similar relative lengths in Microcebus species,
but not significantly different from those in species
of Cheirogaleus (Table 3a).
E. elegantulus exhibits significantly lower condyle
height shapes and relatively longer AP temporal
articular lengths in all of the comparisons with
nongouging galagids (Table 3b). In many compari-
160
C.J. VINYARD ET AL.
similar between E. elegantulus and nongouging galagids (Table 3b).
C. jacchus exhibits the most shape differences predicted to facilitate large gapes (Table 3c). Shape
variables for condyle height, AP temporal articular
surface length, and masseter origin-insertion ratio
show the predicted morphological differences in
all comparisons of C. jacchus to nongouging callitrichids (Table 3c). For relative AP mandible and
condyle length, C. jacchus shows the predicted difference in one comparison, but only approaches significance in a second comparison to a nongouging
callitrichid (Table 3c).
Because C. jacchus has a significantly longer relative mandible length than Leontopithecus rosalia
(Table 3c), using mandible length as the denominator in our biomechanical shape variables may generate different results than shape variables created
using an overall size estimate such as a GM. Among
the 13 shape variables, this influence of mandible
length appears to be an issue for hypothesis-testing
in the comparison of AP condyle length shape. In
fact, C. jacchus has a significantly longer relative AP
condyle length than L. rosalia when using our GM
as a size estimate.
DISCUSSION
Skull morphology and gouging forces
Fig. 1. Box plots of condyle height shape, relative to mandible
length, for (A) Phaner furcifer and other nongouging cheirogaleids, (B) Euoticus elegantulus and nongouging galagids, and (C)
Callithrix jacchus vs. nongouging callitrichids. For each family or
subfamily, the gouging species has a significantly lower condyle
height shape when compared to each of the nongouging taxa in
that group. Line within box denotes median. Boundaries of box
represent 25th and 75th percentiles. Whiskers indicate 10th and
90th percentiles. Solid circles denote 5th and 95th percentiles.
Complete species designations are given in Table 1.
sons, E.elegantulus has significantly longer relative
AP condyle lengths. Both relative AP mandible
length and the masseter origin-insertion ratio are
Many researchers have suggested that gouging
primates generate relatively large external forces on
the jaw and large internal loads in the skull during
gouging (Szalay and Seligsohn, 1977; Szalay and
Delson, 1979; Rosenberger, 1992; Dumont, 1997;
Williams and Wall, 1999; Spencer, 1999; Vinyard,
1999). Furthermore, skull shapes in gouging primates have been linked functionally to these hypothesized forces and loads (e.g., Dumont, 1997).
Our results suggest that gouging primates exhibit
few of the predicted skull morphologies that should
be linked to large gouging forces and loads. These
findings certainly do not exclude there being large
forces at the jaw during gouging in these species.
Indeed, we did not consider other relevant factors
such as the distribution of compact bone in the mandibular corpus and symphysis, jaw muscle sizes, or
internal muscle architecture. Finally, it is also possible that larger samples, and hence greater statistical power, might allow us to identify smaller, yet
still statistically significant, differences in skull
form linked to gouging forces.
Among the three gouging species we examined,
Euoticus elegantulus shows the largest number of
mandibular shapes predicted to offer increased resistance to internal loads in the jaw during gouging
(i.e., predictions 1– 4; Table 3b). However, there is no
immediately apparent pattern to these predicted
mandibular shapes either within or among galagid
species. For example, each of these four mandibular
shapes is significantly larger in E. elegantulus vs.
SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES
161
Galago moholi, but none differ from analogous
shapes in Galagoides gallarum. This inconsistency
makes it hard to interpret the functional significance of mandibular shapes in E. elegantulus. This
difficulty is compounded by some uncertainty concerning how E. elegantulus extracts gums and the
frequency of gouging during gum feeding (e.g.,
Charles-Dominique and Petter, 1980). We also cannot rule out that other feeding behaviors, unrelated
to exudate feeding, are responsible for the robust
jaws of E. elegantulus relative to some galagids. Our
comparative results are sufficiently interesting to
merit further behavioral and morphological research to clarify the relationship between jaw form,
gouging, and feeding ecology in E. elegantulus.
Comparing functional interpretations of skull
form in gouging primates
Dumont (1997) conducted the first comparative
study of skull shapes in tree-gouging primates. She
examined E. elegantulus, C. jacchus, and Cebuella
pygmaea in the context of a wider range of gouging
and nongouging mammals than examined here. Dumont (1997) described these gouging species as having higher condyles above the occlusal plane, shorter
mandibles, and wider crania in the temporal fossa
and nuchal regions relative to a skull GM as compared to frugivorous and nectivorous bats, marsupials, and primates. Gougers are also reported to have
shorter relative AP condyle lengths when compared
to these frugivores (Dumont, 1997). Based on the
assumption that gouging involves high forces, these
shape differences were interpreted by Dumont
(1997) to provide greater force production or offer
increased resistance in the skull to the elevated
internal loads linked to gouging.
Our analysis of skull shape in gouging primates
gives several results that contradict the morphological findings reported by Dumont (1997). One difference is that the three gouging species we consider,
including two studied by Dumont (1997), have low
condyle heights relative to mandible length in all
comparisons with nongouging species (Fig. 2). Contrary to Dumont (1997), we find mandible lengths
relative to a skull GM to be statistically similar in
gougers as compared to closely related nongougers,
with the exception of one case where the gouging
species has a significantly longer mandible (Table
3c). We found that Callithrix jacchus has relatively
wider crania in the temporal fossa region (MCW) vs.
other callitrichids, as suggested by Dumont (1997).
The two strepsirrhine gougers, however, have similar or significantly narrower relative minimum cranial widths when compared to nongougers of the
same family. Finally, the AP length of the condyle
relative to mandible length is either not different or
is significantly longer in gouging species.
We identify three potential, nonmutually exclusive, explanations for these two contrasting reports
of skull shapes in gouging primates. First, the two
Fig. 2. Lateral views of mandibles for (A) Phaner furcifer and
Cheirogaleus major, (B) Euoticus elegantulus and Galagoides
demidoff, and (C) Callithrix jacchus and Saguinus fuscicollis. In
A–C, the gouging species shows a condyle that is positioned
lower, closer to the toothrow, in comparison with the nongouging
species. Scale bar, 1 cm. Adapted from Hershkovitz (1977).
studies do not examine precisely the same gouging
primates. We do not include C. pygmaea, while Dumont (1997) did not analyze P. furcifer. Both studies
did, however, include E. elegantulus and C. jacchus.
Nevertheless, all three gouging taxa in our study
show a basically similar pattern of comparative results for these skull shapes.
Second, the two studies use different comparative
samples. Given that the conclusions regarding skull
shape in gouging primates are relative to the comparative sample, the different samples are likely to
be a major factor underlying the dissimilar morphologies reported by the two studies. We examine skull
shapes in gouging primates relative to closely related, nongouging taxa in the same family or subfamily. Dumont (1997) compared skull shapes in
tree gougers to other species of primates, bats, and
marsupials. We argue that the broad taxonomic
sampling used by Dumont (1997) makes it difficult
to identify morphological features functionally related to tree gouging vs. morphological variability
related to the separate phylogenetic history of these
different taxa (Fleagle, 1977a,b, 1978; Szalay and
162
C.J. VINYARD ET AL.
Delson, 1979; Felsenstein, 1985; Huey and Bennett,
1986, 1990; Bennett and Huey, 1990; Garland and
Adolph, 1994; Harvey and Pagel, 1991; Miles and
Dunham, 1993). If the goal is to identify morphological changes in the skull related to gouging in a
specific tree-gouging species, then it is preferable to
compare the gouging species to closely related nongouging taxa.
In effect, we are arguing that a comparative morphometric study aimed at identifying form-function
relationships in a particular species performing a
derived behavior is best accomplished by comparing
this species to closely related species that span the
presumed behavioral shift (see Coddington, 1988).
This approach maximizes the form-function “signal”
to unrelated phylogenetic “noise” ratio. Furthermore, this method mimics the empirically powerful
approach applied in studying the effects of artificial
selection where the populations before and after selection are compared to quantify selection. We make
three sets of these comparisons. By comparing multiple gouging species to their closely related nongouging relatives, we are able to assess morphological
convergence, or the lack thereof, in tree-gouging primates. The convergent reduction of relative condyle
height in all three gouging species bolsters our functional hypothesis linking this morphological change
with large jaw gapes associated with tree gouging.
Lack of convergence, however, should not be interpreted as evidence that a predicted morphological
change observed in one gouging species, such as the
increased masseter origin-insertion ratio in C. jacchus, is unimportant for that species simply because
it is not observed in other gougers.
Our use of this comparative approach gives rise to
at least two concerns that need to be addressed.
First, we are arguably violating the spirit of our
method outlined in the previous paragraph by comparing each species of interest to multiple comparative taxa within a family or subfamily, when in fact
comparison to the sister taxon is really most appropriate. Unfortunately, we cannot at present definitively identify the appropriate sister taxon for most
of the gouging species. For example, P. furcifer is
identified as the sister taxon to all other cheirogaleids by Yoder (1997). More importantly, we do not
know whether the extant sister taxa exhibit the
morphology found in the nongouging ancestor of our
species of interest. Therefore, we maintain that our
criteria requiring a predictable change in multiple
comparisons with closely related species offer a rigorous, albeit conservative, test of form-function relationship. A second concern relates to the fact that
each gouging species is compared to a different number of nongouging taxa. These varying numbers of
comparisons raise the question of whether there are
differences in the power of the tests among the three
gouging species. We can neither confirm nor reject
this issue, based on the observed results.
We want to be extremely careful to point out that
we are not rejecting all broad, interspecific approaches to studying form and function with morphometric data. The utility and importance of interspecific allometric studies, for example, have been
demonstrated numerous times. We simply argue
that questions about form-function relationships in
a particular species, or a clade, exhibiting a specific
behavior may be better addressed when using morphometric data by comparing that group to a closely
related one that does not perform that particular
behavior.
Third, the two studies use different denominators
in calculating shape variables. Dumont (1997) used
a geometric mean of several skull measurements to
estimate skull size. We used mandible length as a
biomechanical standard in most cases. Given that a
shape is calculated relative to some other measure,
different relative criteria will result in divergent
shape estimates for the same morphology (Mosimann and James, 1979). This difference in calculating shape variables likely contributes to the contrasting results of the two studies (see Appendix).
We agree with Dumont (1997) that fossil gougers
can be identified using skull shapes derived from a
generalized skull size estimate such as a geometric
mean of skull dimensions. We are not attempting
this kind of allometric analysis of skull form in gouging primates, and therefore we are not trying to
describe size-related changes in skull shapes among
gouging and nongouging primates. However, we
contend that it may be problematic to develop functional interpretations of skull shapes derived from
these general skull size estimates, because they do
not directly consider relevant mechanical factors affecting skull functions during gouging. We argue
that the biomechanical significance of mandible
length for force- and gape-related jaw functions
makes it a more appropriate estimate for addressing
skull form-function relationships in gouging primates. From a functional perspective, it is the relationship between the two mechanically relevant
components of the shape variable that is important
for understanding skull function during gouging,
and it is less relevant to identify which component(s)
of the shape variable is changing with size. By contrasting our approach with that of Dumont (1997),
we are revisiting an old argument debating the appropriateness of size adjustment with overall size
estimates vs. relevant biomechanical standards in
studying jaw biomechanics (cf. Smith, 1983, 1993 to
Hylander, 1985, 1988; Bouvier, 1986a; Daegling,
1989; Ravosa, 1991, 1996b). In general, if a biomechanical relationship can be identified, then we suggest shapes should also be examined relative to a
biomechanical standard before making functional
interpretations.
Our morphological findings challenge two of the
conclusions made by Dumont (1997) based on her
analysis of skull shapes. First, her argument that
SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES
gouging primates have increased force production
abilities through both improved leverage for gouging
and larger jaw-muscle attachment areas, as well as
increased load resistance in their skulls, must be
viewed with caution. In vivo data on jaw forces during gouging are needed before we can reliably interpret skull form-function associations in gouging primates. Second, the classification functions Dumont
(1997) recommended for identifying tree gouging in
fossil primates may not be as useful as previously
stated. This is because the combined results of these
two analyses show that the interpretation of skull
shapes in gouging primates is highly contingent on
the comparative sample.
Skull form and jaw gapes during gouging
While several researchers have speculated about
gouging forces in the skull, the potential importance
of jaw movements during gouging, as estimated by
jaw gapes, has been largely overlooked. We have
observed common marmosets in a laboratory setting
using larger gapes during gouging than during
chewing (Vinyard et al., 2001, and unpublished
data). We examined whether gouging primate species exhibit morphologies that facilitate large gapes
based on these preliminary observations. When
compared to closely related nongouging primates,
each gouging species does possess skull shapes that
likely increase jaw gapes. Thus, we hypothesize that
these derived skull shapes in gouging primates are
functionally related to the need for relatively large
gapes during gouging.
Many researchers have addressed the importance
of gape in mammalian skull functional morphology
(e.g., Wolff-Exalto, 1951; Moss, 1968; Herring, 1972,
1975; Greaves, 1974, 1995; Herring and Herring,
1974; Hylander, 1979b; Emerson and Radinsky,
1980; Lucas, 1981, 1982; Smith, 1984; Joeckel, 1990;
Ravosa, 1990; Jablonski, 1993; Jablonski and
Crompton, 1994). These efforts functionally link
large gapes to display behaviors, prey capture, fighting, slashing, incising large-diameter foods, and
crushing large-diameter foods at the posterior teeth.
Our results imply that tree gouging in primates may
be another behavior necessitating large gapes.
All three gouging species consistently display
relatively low condyle heights when compared to
closely related nongouging species (Fig. 2). Condyle
heights vary dramatically among primates. This
variability appears to be correlated with differences
in diet, feeding behavior, canine displays, and fighting (e.g., Zingeser, 1973; Hylander, 1979b; Ward and
Molnar, 1980; Lucas, 1981, 1982; Ravosa, 1990; Jablonski, 1993; Ravosa et al., 2000). A cursory glance
at the skulls of living primates suggests that relatively high condyles above the occlusal plane occur
in folivorous species (e.g., Alouatta and Brachyteles
in contrast to Ateles) and relatively low condyles are
found in species that use wide gapes during canine
displays (e.g., Papio and Mandrillus in comparison
163
to Theropithecus). Our findings suggest that treegouging primates may offer additional evidence relating low relative condyle heights and wide gapes in
primates.
Variation in condyle heights has functional relevance for activities involving the oral apparatus.
Many researchers consider high condyles above the
toothrow advantageous for powerful and repetitive
mastication by increasing attachment areas and
lengthening the moment arms for the masseters and
medial pterygoids, as well as distributing occlusal
forces more evenly across the postcanine teeth
(Wolff-Exalto, 1951; Maynard Smith and Savage,
1959; Davis, 1964; Turnbull, 1970; Greaves, 1974;
Ward and Molnar, 1980). Low condyles are thought
to decrease stretching of the masseters and medial
pterygoids during jaw opening, reduce posterior displacements of the mandible during opening, and
increase the temporalis moment arm (assuming
coronoid height remains constant) (Herring, 1972,
1975; Herring and Herring, 1974).
We identify two potential functional benefits of a
low condyle relative to the mandibular toothrow in
the context of tree gouging at large gapes. First, low
condyles may aid bite force production at the anterior teeth during gouging. The jaw muscles elongate
as the mouth opens. Empirical data in primates
indicate that bite-force production diminishes as
jaw-muscle fibers stretch beyond their resting
length during jaw opening (Dechow and Carlson,
1982, 1986, 1990). Bite force reduction due to muscular stretching is further compounded by the relatively inefficient jaw-lever relationships for producing forces at the anterior teeth. Therefore, gougers
that need to generate bite forces at large gapes
would be under pressure to minimize stretching of
jaw-muscle fibers at these large gapes. A low condyle
reduces jaw muscle stretching at a given gape and
provides one structural solution to this problem
(Herring and Herring, 1974).
A second potential benefit of a low condyle with
respect to the occlusal plane relates to reducing the
posterior displacement of the mandible at large
gapes. Relative to the upper teeth, the lower anterior teeth move inferiorly and posteriorly during jaw
opening. Lowering the height of the condyle relative
to the mandibular toothrow reduces the amount of
posterior displacement of these teeth for a given
degree of jaw rotation (Davis, 1964; Herring, 1972;
Lucas, 1981, 1982). If the lower anterior teeth are
displaced too far posteriorly at large gapes during
gouging, then it may be difficult to position the cutting edge of these teeth at an appropriate angle
relative to the gouging substrate. Thus, we speculate that a low condyle height may be important for
the effective alignment of the anterior teeth during
gouging at large gapes.
The anteroposterior (AP) lengths of the condyle and
temporal articular surfaces are significantly longer in
specific gouging primates relative to closely related
164
C.J. VINYARD ET AL.
nongougers at a given size. For example, relative condyle length in P. furcifer is significantly longer than all
cheirogaleids sampled, whereas E. elegantulus and C.
jacchus have significantly longer relative temporal articular surfaces than all other species in their respective family or subfamily. Cineradiographic studies indicate that during jaw opening in primates, the
condyle rotates about an approximate mediolateral
axis and translates anteriorly along the temporal articular surface (Hiiemae and Kay, 1973; Kay and
Hiiemae, 1974a,b; Hylander, 1978; Hylander et al.,
1987; Wall, 1999). Wall (1999) further demonstrated
that condylar rotation and translation are correlated
with gape during jaw opening. AP lengthening of the
condyle increases potential gapes by increasing the
range of possible rotational excursion in the mandible
(cf. Currey, 1984; Ruff, 1988; Hamrick, 1996). A longer
temporal articulation increases the translational surface for the condyle during jaw opening. Thus, relative
lengthening of these TMJ articular surfaces will provide increased gape potentials in gouging primates. In
addition, the relatively elongated condyles of gouging
primates may reduce stresses (i.e., force/area) in the
TMJ during gouging by increasing relative condyle
area.
We stress that these results provide only preliminary support linking skull form, relatively large gapes,
and gouging. Our comparative study only examined
jaw shape and craniometric correlates of masseter
(and assumably medial pterygoid) stretching, condylar
rotation, and translation as they relate to large gapes.
We did not consider stretching of the temporalis (e.g.,
Herring and Herring, 1974; Emerson and Radinsky,
1980; Joeckel, 1990; Ravosa, 1990). Furthermore, we
did not examine jaw-muscle fiber lengths, even though
it is well-known that the tension produced by a muscle
fiber decreases as that fiber is stretched beyond an
optimum length (e.g., Ramsey and Street, 1940; Hill,
1953; Gans and Bock, 1965; Gordon et al., 1966; Herring and Herring, 1974; Anapol and Herring, 1989).
We also did not look at other soft-tissue components
that might limit jaw gapes.
Finally, we have not provided a compelling explanation of the functional benefit(s) of relatively large
gapes during tree gouging. Perhaps large gapes are
advantageous for optimal alignment of the incisal
cutting edges for penetrating the tree substrate. A
large gape also signifies a greater amount of anterior
tooth movement during closing for removing isolated tree pieces. Additionally, changes in skull form
that reduce jaw muscle stretching for a given gape
theoretically will increase jaw muscle force production at that gape. We intend to address the functional
significance of large gapes for gouging through in vivo
analyses of gouging mechanics in Callithrix jacchus.
Inferring gouging functions from comparative
studies of skull form
We implicitly assumed at the outset of this study
that gouging involves larger jaw forces and/or larger
jaw gapes relative to other behaviors involving the
oral apparatus. We did this to determine if there are
predictable changes in skull morphology in gouging
primates that may be functionally related to these
purported large forces and/or gapes during gouging.
This assumption was necessary because there currently are only preliminary in vivo data pointing to
the magnitudes of jaw forces and jaw gapes during
gouging (Vinyard et al., 2001).
We would like to apply the comparative morphological results presented here to address those hypotheses stating that jaw forces and jaw gapes are
relatively large during gouging. However, we cannot
conclusively address force- and gape-related functions during gouging with our morphometric data
because of the two additional assumptions we made
in this analysis. First, we assumed that skull form
responds to these hypothesized functional demands.
This assumption is common in comparative morphological studies of the skull, and is bolstered by in
vivo data during mastication, incision, and biting
that suggest jaw form and function are linked (Hylander, 1979a,b, 1984, 1985, 1988; Daegling and Hylander, 1997; Hylander et al., 1998, 2000). However,
it has been convincingly argued and empirically
demonstrated that form and function are not always
closely linked in organisms (Bock, 1977, 1989;
Lauder, 1995, 1996). Because of the lack of a strict,
law-like relationship between form and function, our
comparative morphometric analysis cannot definitively address whether jaw forces and/or jaw gapes
during gouging are relatively large.
Second, we assumed that incision and anterior
tooth biting provide reasonable functional models
for inferring the external forces at the jaw and internal loads in the skull as well as jaw movements
during gouging. For example, this assumption allowed us to apply in vivo data from primate incision
and anterior tooth biting to infer morphological responses to the hypothesized large external forces
during gouging (see predictions 1– 4). Similarly, we
assumed that jaw-opening movements during gouging involved jaw rotations and translations that are
comparable to those observed during jaw opening for
incision.
The demonstration of a steep strain gradient in
the macaque zygomatic arch by Hylander and Johnson (1997) highlights why inferring functions in primate skulls can be problematic. They showed that
during chewing, the anterior portion of the macaque
zygomatic arch exhibits higher strains relative to
the intermediate strains in the middle portion of the
arch and even lower strains in the posterior region of
the arch. If we accept that the anterior portion of the
arch is near optimized for resisting masticatory
stresses,6 then the more posterior sections of the
6
In other words, the anterior portion of the zygomatic arch exhibits
near-maximum strength with a minimum amount of tissue.
SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES
arch could be significantly reduced in size without
compromising their load-resisting ability during
chewing (Hylander and Johnson, 1997). Similar
strain gradients during mastication have been
shown throughout other areas of the macaque skull
(Hylander et al., 1991; Hylander and Johnson, 1992;
Ross, 2001). These gradients, coupled with the observation that form cannot predict masticatory
stresses across the macaque mandible (Daegling,
1993), indicate that we cannot routinely determine
function in primate skulls simply from observing
skull form. However, comparative morphological
studies of primate skulls still may be able to assess
variation in function correctly, so long as in vivo
data for at least one primate species demonstrate
that a form-function relationship exists. Given the
scarcity of in vivo data on jaw forces and gapes
during gouging, we cannot definitively link form to
function in this comparative analysis.
Having stated the limitations imposed by our assumptions, we consider this comparative morphological analysis to be a reasonable first step in addressing these two functional hypotheses. We argued at
the outset of this study that if a gouging species
exhibits the predicted morphology in all comparisons with the nongouging species in its family or
subfamily, then correlational support suggests that
a particular skull form is functionally linked to
gouging in that species. We currently are measuring
the jaw forces and jaw gapes during gouging in
Callithrix jacchus. These in vivo data will provide an
empirical description of jaw mechanics during gouging and test the respective hypotheses that gouging
is associated with large jaw forces and/or large jaw
gapes relative to other behaviors involving the oral
apparatus. Based on the results from this comparative morphometric analysis, we predict that jaw
forces during gouging will not be relatively large,
and therefore will not result in relatively large internal skull loads in comparison to forces associated
with other voluntary activities. We also predict that
maximum jaw gapes will be relatively large during
gouging, and that gouging primates are able to open
their jaws relatively wider than closely related
nongouging species.
CONCLUSIONS
Our analysis of the skull shapes of Phaner furcifer, Euoticus elegantulus, and Callithrix jacchus indicate little evidence to suggest that these species
have a greater ability either to generate force at the
anterior teeth or to resist loads in the skull when
compared to closely related nongouging species.
Based on these morphological comparisons, we pre-
165
dict that forces in the jaw during gouging will be
similar to or less than forces during other activities
involving the oral apparatus. This prediction is a
significant departure from previous speculations
that forces are relatively high in the skull during
gouging. We also show that these three gouging
species possess several skull shapes that facilitate
larger gapes. We predict that tree gouging will involve maximum gapes that are relatively larger
than maximum gapes during other behaviors involving the oral apparatus.
The theoretical foundation guiding decisions
about comparative samples and shape variables for
comparative morphometric research has received
considerable attention (e.g., Mosimann and James,
1979; Harvey and Pagel, 1991; Jungers et al., 1995).
Contrasting the findings of our study with those of
Dumont (1997) provides a clear example of how the
choice of a comparative sample and/or denominator
of a shape variable can impact the results of comparative morphometric research. These two studies
generate dissimilar results and hence offer widely
different functional interpretations of skull form for
essentially the same species of gouging primates.
Clearly both studies cannot be correct in their interpretations of skull form-function relationships.
While we obviously favor our decisions regarding
comparative samples and the choice of shape variables, we strongly recommend that an in vivo approach must provide the foundation for determining
jaw functions. In this instance, in vivo data are
necessary to empirically establish jaw force- and
gape-related functions during gouging.
ACKNOWLEDGMENTS
We thank the following institutions and individuals for providing access to primate skulls: Field Museum of Natural History (L. Heaney, B. Patterson,
and W. Stanley); National Museum of Natural History (L. Gordon and R. Thorington); American Museum of Natural History (R. MacPhee); Natural
History Museum, London (P. Jenkins); Muséum National d’Histoire Naturelle (J. Cuisin); Naturhistorisches Museum Basel (M. Sutermeister and F. Weidenmayer). B. Shea and D. Schmitt kindly allowed
access to video capture and videometric analysis
software. We thank K. Johnson, C. Kirk, P. Lemelin,
B. Payseur, D. Schmitt, and P. Vinyard for numerous helpful discussions and comments that greatly
improved the manuscript. Funding for collection of
morphometric data was provided by Sigma-Xi, the
Boise Fund, the AMNH, the NSF (SBR-9701425),
and the L.S.B. Leakey Foundation.
166
C.J. VINYARD ET AL.
APPENDIX
At the request of multiple reviewers and the editor, we have included the results of pairwise species
comparisons of skull shapes created with a geometric mean of 11 skull measurements (defined in Table 2)
as the denominator in each shape variable for (a) Phaner furcifer vs. other cheirogaleids, (b) Euoticus
elegantulus vs. other galagids, and (c) Callithrix jacchus vs. other callitrichids. We maintain that our use
of a biomechanical standard to hold constant specific aspects of the biomechanical system we are studying
is an important, and in many ways preferred, method of looking at the functional consequences of skull form
in tree-gouging primates. That having been said, we agree with the reviewers and editor that it is important
to be able to compare results that use different denominators in shape variables. We strongly caution,
however, about extrapolating any conclusions from this comparison to size adjustment techniques in
general. This concern is warranted, because creating shape variables using different geometric means in the
denominator results in different interpretations of skull form in gouging primates. See Table 3 for
explanatory footnotes. We omitted mandible length, AP mandible length, and masseter origin-insertion
ratio in the Appendix because the shape variables are the same as those in Table 3. The numbering of shape
variable comparisons is consistent with Table 3.
a. P. furcifer vs. cheirogaleids
Shape variable
Cheirogaleus
major
Cheirogaleus
medius
Microcebus
murinus
Microcebus
rufus
Mirza
coquereli
1. M1 depth (Pf ⬎)
2. M1 width (Pf ⬎)
3. Symphysis length (Pf )
4. Condyle area (Pf ⬎)
5. Minimum cranial width (Pf ⬎)
6. Mandible length (Pf⬍)
8. Masseter moment arm (Pf ⬎)
9. AP mandible length (Pf ⬎)
10. Condyle height (Pf ⬍)
12. Condyle length (Pf⬎)
13. Temporal articular surface length (Pf⬎)
Ns/Ns
0.04/Ns
0.009/Ns
Ns/Ns
Ns/Ns
Ns/Ns
Ns/Ns
Ns/Ns
0.03/Ns
0.04/Ns
0.003/⫺
Ns/Ns
Ns/Ns
0.002/⫺
Ns/Ns
Ns/Ns
Ns/Ns
0.01/Ns
Ns/Ns
0.003/⫺
0.004/⫺
0.03/Ns
Ns/Ns
Ns/Ns
0.004/⫺
0.004/⫺
Ns/Ns
Ns/Ns
Ns/Ns
Ns/Ns
0.0007/⫺
0.001/⫺
0.001/⫺
0.02/Ns
Ns/Ns
0.001/⫺
0.009/Ns
Ns/Ns
0.04/Ns
Ns/Ns
Ns/Ns
0.002/⫺
0.001/⫺
0.02/Ns
Ns/Ns
Ns/Ns
0.008/Ns
0.003/⫺
Ns/Ns
Ns/Ns
Ns/Ns
Ns/Ns
0.002/⫺
0.001/⫺
0.004/⫺
b. E. elegantulus vs. galagids
Shape variable
Galagoides
alleni
Galago
moholi
Galago
senegalensis
Galagoides
zanzibaricus
Galagoides
demidoff
Galagoides
gallarum
1. M1 depth (Ee⬎)
2. M1 width (Ee⬎)
3. Symphysis length (Ee⬎)
4. Condyle area (Ee⬎)
5. Minimum cranial width (Ee⬎)
6. Mandible length (Ee⬍)
8. Masseter moment arm (Ee⬎)
9. AP mandible length (Ee⬎)
10. Condyle height (Ee⬍)
12. Condyle length (Ee⬎)
13. Temporal articular surface length (Ee⬎)
0.0001/⫺
0.009/⫺
0.00004/⫺
0.00009/⫺
Ns/Ns
Ns/Ns
0.002/⫺
Ns/0.01
0.00002/⫺
0.0002/⫺
0.000007/⫺
0.0007/⫺
0.00001/⫺
0.00001/⫺
0.001/⫺
Ns/0.0002
Ns/0.02
0.003/⫺
0.02/Ns
0.000008/⫺
0.006/⫺
0.00003/⫺
0.00007/⫺
0.007/⫺
0.00001/⫺
0.002/⫺
Ns/0.008
Ns/0.02
0.0008/⫺
Ns/Ns
0.000006/⫺
Ns/Ns
0.0004/⫺
0.0001/⫺
0.03/Ns
0.0002/⫺
0.002/⫺
Ns/Ns
Ns/Ns
Ns/Ns
Ns/0.02
0.00007/⫺
0.003/⫺
0.001/⫺
0.00003/⫺
0.000003/⫺
0.01/Ns
0.007/⫺
Ns/0.02
Ns/Ns
0.00009/⫺
Ns/Ns
0.00009/⫺
0.03/Ns
0.000004/⫺
0.003/⫺
0.007/⫺
0.004/⫺
Ns/Ns
Ns/Ns
Ns/0.006
Ns/Ns
0.01/Ns
0.0004/⫺
Ns/Ns
0.0001/⫺
c. C. jacchus vs. callitrichids
Shape variable
1. M1 depth (Cj⬎)
2. M1 width (Cj⬎)
3. Symphysis length (Cj⬎)
4. Condyle area (Cj⬎)
5. Minimum cranial width (Cj⬎)
6. Mandible length (Cj⬍)
8. Masseter moment arm (Cj⬎)
9. AP mandible length (Cj⬎)
10. Condyle height (Cj⬍)
12. Condyle length (Cj⬎)
13. Temporal articular surface length (Cj⬎)
Leontopithecus rosalia
Saguinus fuscicollis
Ns/0.02
Ns/0.0009
Ns/Ns
Ns/Ns
0.00002/⫺
Ns/0.006
Ns/Ns
0.004/⫺
0.000007/⫺
0.002/⫺
0.000005/⫺
Ns/0.04
Ns/0.0005
Ns/0.0003
Ns/Ns
0.005/⫺
0.04/Ns
Ns/0.03
0.02/Ns
0.000007/⫺
0.0002/⫺
0.000001/⫺
SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES
167
LITERATURE CITED
Anapol F, Herring SW. 1989. Length-tension relationships of
masseter and digastric muscles of miniature swine during ontogeny. J Exp Biol 143:1–16.
Bearder SK, Martin RD. 1980. Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). Int J Primatol 1:103–128.
Bennett AF, Huey RB. 1990. Studying the evolution of physiological performance. In: Futuyma D, Antonovics J, editors. Oxford
surveys in evolutionary biology. Volume 7. Oxford: Oxford University Press. p 251–284.
Bock WJ. 1977. Adaptation and the comparative method. In:
Hecht MK, Goody PC, Hecht BM, editors. Major patterns in
vertebrate evolution. New York: Plenum Press. p 57– 82.
Bock WJ. 1989. Principles of biological comparison. Acta Morphol
Neerl Scand 27:17–32.
Bouvier M. 1986a. A biomechanical analysis of mandibular scaling in Old World monkeys. Am J Phys Anthropol 69:473– 482.
Bouvier M. 1986b. Biomechanical scaling of mandibular dimensions in New World monkeys. Int J Primatol 7:551–567.
Brooks DR, McLennan DA. 1991. Phylogeny, ecology and behavior: a research program in comparative biology. Chicago: University of Chicago Press.
Charles-Dominique P. 1974. Ecology and feeding behaviour of five
sympatric lorisids in Gabon. In: Martin RD, Doyle GA, Walker
AC, editors. Prosimian biology. London: Duckworth Press.
p 131–150.
Charles-Dominique P. 1977. Ecology and behaviour of nocturnal
primates. London: Duckworth Press.
Charles-Dominique P, Bearder SK. 1979. Field studies of lorisid
behavior: methodological aspects. In: Doyle GA, RD Martin,
editors. The study of prosimian behavior. New York: Academic
Press. p 567– 629.
Charles-Dominique P, Petter JJ. 1980. Ecology and social life of
Phaner furcifer. In: Charles-Dominique P, Cooper HM, Hladik
A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A,
Schilling A, Petter JJ, editors. Nocturnal Malagasy primates:
ecology, physiology and behavior. New York: Academic Press.
p 75–96.
Chivers DJ, Hladik CM. 1980. Morphology of the gastrointestinal
tract in primates: comparisons with other mammals in relation
to diet. J Morphol 166:337–386.
Chivers DJ, Hladik CM. 1984. Diet and gut morphology in primates. In: Chivers DJ, Wood BA, Bilsborough A, editors. Food
acquisition and processing in primates. New York: Plenum
Press. p 213–230.
Coddington JA. 1988. Cladistic tests of adaptational hypotheses.
Cladistics :43–22.
Coimbra-Filho AF, Mittermeier RA. 1976. Exudate-eating and
tree-gouging in marmosets. Nature 262:630.
Coimbra-Filho AF, Mittermeier RA. 1977. Tree-gouging, exudateeating and the “short-tusked” condition in Callithrix and Cebuella. In: Kleiman DG, editor. The biology and conservation of
the Callitrichidae. Washington, DC: Smithsonian Institution
Press. p 105–115.
Coimbra-Filho AF, Da Cruz Rocha N, Pissinatti A. 1980. Morfofisiologia do ceco e sua correlacao com o tipo odontologico em
callitrichidae (Platyrrhini, Primates). Rev Bras Biol 40:177–
185.
Cole TM. 1992. Postnatal heterochrony of the masticatory apparatus in Cebus apella and Cebus albifrons. J Hum Evol 23:253–
282.
Currey J. 1984. The mechanical adaptations of bones. Princeton:
Princeton University Press.
Daegling DJ. 1989. Biomechanics of cross-sectional size and
shape in the hominoid mandibular corpus. Am J Phys Anthropol 80:91–106.
Daegling DJ. 1992. Mandibular morphology and diet in the genus
Cebus. Int J Primatol 13:545–570.
Daegling DJ. 1993. The relationship of in vivo bone strain to
mandibular corpus morphology in Macaca fascicularis. J Hum
Evol 25:247–269.
Daegling DJ, Hylander WL. 1997. Occlusal forces and mandibular bone strain: is the primate jaw “overdesigned”? J Hum Evol
33:705–717.
Darroch JN, Mosimann JE. 1985. Canonical and principal components of shape. Biometrika 72:241–252.
Davis DD. 1964. The giant panda: a morphological study of evolutionary mechanisms. Fieldiana Zool Mem 3:1–339.
Dechow PC, Carlson DS. 1982. Bite force and gape in rhesus
monkeys. Am J Phys Anthropol 57:179.
Dechow PC, Carlson DS. 1986. Growth, gape and jaw mechanics
in rhesus monkeys. Am J Phys Anthropol 69:193.
Dechow PC, Carlson DS. 1990. Occlusal force and craniofacial
biomechanics during growth in rhesus monkeys. Am J Phys
Anthropol 83:219 –237.
Dumont ER. 1997. Cranial shape in fruit, nectar, and exudate
feeders: implications for interpreting the fossil record. Am J
Phys Anthropol 102:187–202.
Eaglen RH. 1986. Morphometrics of the anterior dentition in
strepsirhine primates. Am J Phys Anthropol 71:185–202.
Emerson SB, Radinsky LB. 1980. Functional analysis of sabertooth cranial morphology. Paleobiology 6:295–312.
Falsetti AB, Jungers WL, Cole TM. 1993. Morphometrics of the
callitrichid forelimb: a case study in size and shape. Int J
Primatol 14:551–572.
Felsenstein J. 1985. Phylogenies and the comparative method.
Am Nat 125:1–15.
Ferrari SF. 1993. Ecological differentiation in the Callitrichidae.
In: Rylands AB, editor. Marmosets and tamarins: systematics,
behaviour, and ecology. Oxford: Oxford University Press.
p 314 –328.
Fleagle JG. 1977a. Locomotor behavior and skeletal anatomy of
sympatric Malaysian leaf-monkeys (Presbytis obscura and
Presbytis melalophos). Yrbk Phys Anthropol 20:440 – 453.
Fleagle JG. 1977b. Locomotor behavior and muscular anatomy of
sympatric Malaysian leaf-monkeys (Presbytis obscura and
Presbytis melalophos). Am J Phys Anthropol 46:297–308.
Fleagle JG. 1978. Locomotion, posture, and habitat utilization in
two sympatric Malaysian leaf-monkeys (Presbytis obscura and
Presbytis melalophos). In: Montgomery GG, editor. The ecology
of arboreal folivores. Washington, DC: Smithsonian Institution
Press. p 243–251.
Fleagle JG. 1999. Primate adaptation and evolution. New York:
Academic Press.
Fonseca GAB, Lacher TE. 1984. Exudate-feeding by Callithrix
jacchus penicillata in semideciduous woodland (cerradao) in
central Brazil. Primates 25:441– 450.
Gans C, Bock WJ. 1965. The functional significance of muscle
architecture—a theoretical analysis. Ergeb Anat Entwick 38:
115–142.
Garber PA. 1980. Locomotor behavior and feeding ecology of the
Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae). Int J Primatol 1:185–201.
Garber PA. 1984. Proposed nutritional importance of plant exudates in the diet of the Panamanian tamarin, Saguinus oedipus
geoffroyi. Int J Primatol 5:1–15.
Garber PA. 1992. Vertical clinging, small body size, and the
evolution of feeding adaptations in the Callitrichinae. Am J
Phys Anthropol 88:469 – 482.
Garland T, Adolph SC. 1994. Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool
67:797– 828.
Gordon AM, Huxley AF, Julian FJ. 1966. The variation in isometric tension with sarcomere length in vertebrate muscle
fibers. J Physiol Lond 184:170 –192.
Greaves WS. 1974. Functional implications of mammalian jaw
joint position. Forma Functio 7:363–376.
168
C.J. VINYARD ET AL.
Greaves WS. 1995. Functional predictions from the theoretical
models of the skull and jaws in reptiles and mammals. In:
Thomason JJ, editor. Functional morphology in vertebrate paleontology. Cambridge: Cambridge University Press. p 99 –115.
Gysi A. 1921. Studies on the leverage problem of the mandible.
Dent Dig 27:74 – 84, 144 –150, 203–208.
Hamrick MW. 1996. Articular size and curvature as determinants of carpal joint mobility and stability in strepsirhine primates. J Morphol 230:113–127.
Hamrick MW. 1998. Functional and adaptive significance of primate pads and claws: evidence from New World anthropoids.
Am J Phys Anthropol 106:113–127.
Harcourt C. 1990. Lemurs of Madagascar and the Comoros.
IUCN red data book. Cambridge: IUCN—The World Conservation Union.
Harvey PH. 1991. Comparing uncertain relationships: the Swedes
revolt. TREE 6:38 –39.
Harvey PH, Pagel MD. 1991. The comparative method in evolutionary biology. Oxford: Oxford University Press.
Herring SW. 1972. The role of canine morphology in the evolutionary divergence of pigs and peccaries. J Mammal 53:500 –
512.
Herring SW. 1975. Adaptations for gape in the hippopotamus and
its relatives. Forma Functio 8:85–100.
Herring SW. 1985. Morphological correlates of masticatory patterns in peccaries and pigs. J Mammal 66:603– 617.
Herring SW, Herring SE. 1974. The superficial masseter and
gape in mammals. Am Nat 108:561–576.
Hershkovitz P. 1977. Living New World primates (Platyrrhini),
with an introduction to primates. Volume 1. Chicago: University of Chicago Press.
Hiiemae KM, Kay RF. 1973. Evolutionary trends in the dynamics
of primate mastication. In: Zingeser MR, editor. Symposia, 4th
International Congress of Primatology, volume 3. Basel:
Karger Press. p 28 – 64.
Hill AV. 1953. The mechanics of active muscle. Proc R Soc Lond
[Biol] 141:104 –117.
Hladik CM. 1979. Diet and ecology of prosimians. In: Doyle GA,
Martin RD, editors. The study of prosimian behavior. New
York: Academic Press. p 307–357.
Hladik CM, Charles-Dominique P, Petter JJ. 1979. Feeding strategies of five nocturnal prosimians in the dry forest of the west
coast of Madagascar. In: Charles-Dominique P, Cooper HM,
Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux
A, Schilling A, Petter JJ, editors. Nocturnal Malagasy primates: ecology, physiology and behavior. New York: Academic
Press. p 41–74.
Huey RB, Bennett AF. 1986. A comparative approach to field and
laboratory studies in evolutionary biology. In: Feder ME,
Lauder GV, editors. Predator-prey relationships: perspectives
and approaches from the study of lower vertebrates. Chicago:
University of Chicago Press. p 82–98.
Huey RB, Bennett AF. 1990. Physiological adjustments to fluctuating thermal environments: an ecological and evolutionary
perspective. In: Morimoto RI, Tissieres A, Georgopoulos C,
editors. Stress proteins in biology and medicine. Cold Spring
Harbor: Cold Spring Harbor Press. p 37–59.
Hylander WL. 1975. The human mandible: lever or link? Am J
Phys Anthropol 43:227–242.
Hylander WL. 1978. Incisal bite force direction in humans and
the functional significance of mammalian mandibular translation. Am J Phys Anthropol 48:1– 8.
Hylander WL. 1979a. Mandibular function in Galago crassicaudatus and Macaca fascicularis: an in vivo approach to stress
analysis. J Morphol 159:253–296.
Hylander WL. 1979b. The functional significance in primate mandibular form. J Morphol 160:223–240.
Hylander WL. 1979c. An experimental analysis of temporomandibular joint reaction forces in macaques. Am J Phys Anthropol
51:433– 456.
Hylander WL. 1984. Stress and strain in the mandibular symphysis of primates: a test of competing hypotheses. Am J Phys
Anthropol 64:1– 46.
Hylander WL. 1985. Mandibular function and biomechanical
stress and scaling. Am Zool 25:315–330.
Hylander WL. 1988. Implications of in vivo experiments for interpreting the functional significance of “robust” australopithecines jaws. In: Grine FE, editor. Evolutionary history of
the robust australopithecines. New York: Gruyter Press. p 55–
83.
Hylander WL, Bays R. 1979. An in-vivo strain-gauge analysis of
squamosal-dentary joint reaction force during mastication and
incision in Macaca mulatta and Macaca fascicularis. Arch Oral
Biol 24:689 – 697.
Hylander WL, Johnson KR. 1985. Temporalis and masseter muscle function during incision in macaques and humans. Int J
Primatol 6:289 –322.
Hylander WL, Johnson KR. 1992. Strain gradients in the craniofacial region of primates. In: Davidovitch Z, editor. The biological mechanisms of tooth movement and craniofacial adaptation. Columbus: Ohio State University College of Dentistry.
p 559 –569.
Hylander WL, Johnson KR. 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.
Hylander WL, Johnson KR, Crompton AW. 1987. Loading patterns and jaw movements during mastication in Macaca fascicularis: a bone-strain, electromyographic, and cineradiographic analysis. Am J Phys Anthropol 72:287–314.
Hylander WL, Picq PG, Johnson KR. 1991. Masticatory-stress
hypotheses and the supraorbital region of primates. Am J Phys
Anthropol 86:1–36.
Hylander WL, Ravosa MJ, Ross CF, Johnson KR. 1998. Mandibular corpus strain in primates: further evidence for a functional
link between symphyseal fusion and jaw-adductor muscle force.
Am J Phys Anthropol 107:257–271.
Hylander WL, Ravosa MJ, Ross CF, Wall CE, Johnson KR. 2000.
Symphyseal fusion and jaw-adductor muscle force: an EMG
study. Am J Phys Anthropol 112:469 – 492.
Jablonski NG. 1993. Evolution of the masticatory apparatus in
Theropithecus. In: Jablonski NG, editor. Theropithecus: the rise
and fall of a primate genus. New York: Cambridge University.
p 299 –329.
Jablonski NG, Crompton RH. 1994. Feeding behavior, mastication, and tooth wear in the western tarsier (Tarsius bancanus).
Int J Primatol 15:29 –59.
Joeckel RM. 1990. A functional interpretation of the masticatory
system and paleoecology of entelodonts. Paleobiology 16:459 –
482.
Jungers WL, Falsetti AB, Wall CE. 1995. Shape, relative size,
and size-adjustments in morphometrics. Yrbk Phys Anthropol
38:137–162.
Kay RF, Hiiemae KM. 1974a. Mastication in Galago crassicaudatus: a cinefluorographic and occlusal study. In: Martin RD,
Doyle G, Walker AC, editors. Prosimian biology. London: Duckworth Press. p 501–530.
Kay RF, Hiiemae KM. 1974b. Movement and tooth use in recent
and fossil primates. Am J Phys Anthropol 40:227–256.
Kinzey WG. 1997. Synopsis of New World primates (16 genera).
In: Kinzey WG, editor. New World primates: ecology, evolution
and behavior. New York: Aldine de Gruyter. p 169 –305.
Kinzey WG, Rosenberger AL, Ramirez M. 1975. Vertical clinging
and leaping in a neotropical anthropoid. Nature 255:327–328.
Lacher TE, Fonseca GAB, Alves C, Magalhaes-Castro B. 1981.
Exudate-eating, scent-marking, and territoriality in wild populations of marmosets. Anim Behav 29:306 –307.
Lacher TE, Fonseca GAB, Alves C, Magalhaes-Castro B. 1984.
Parasitism of trees by marmosets in a central Brazilian gallery
forest. Biotropica 16:202–209.
Lauder GV. 1995. On the inference of function from structure. In:
Thomason JJ, editor. Functional morphology in vertebrate paleontology. Cambridge: Cambridge University Press. p 1–18.
Lauder GV. 1996. The argument from design. In: Rose MR,
Lauder GV, editors. Adaptation. New York: Academic Press.
p 55–91.
SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES
Lucas PW. 1981. An analysis of canine size and jaw shape in some
Old and New World non-human primates. J Zool Lond 195:
437– 448.
Lucas PW. 1982. An analysis of the canine tooth size of Old World
higher primates in relation to mandibular length and body
weight. Arch Oral Biol 27:493– 496.
Maddison WP. 2000. Testing character correlation using pairwise
comparisons on a phylogeny. J Theor Biol 202:195–204.
Maier W, Alonso C, Langguth A. 1982. Field observations on
Callithrix jacchus jacchus. Z Saugetierkd 47:334 –346.
Martin RD. 1972. Adaptive radiation and behavior of the Malagasy lemurs. Philos Trans R Soc Lond [Biol] 264:295–352.
Martin RD. 1979. Phylogenetic aspects of prosimian behavior. In:
Doyle GA, Martin RD, editors. The study of prosimian behavior. New York: Academic Press. p 45–77.
Martin RD. 1990. Primate origins and evolution: a phylogenetic
reconstruction. Princeton: Princeton University Press.
Maynard Smith J, Savage RJG. 1959. The mechanics of mammalian jaws. Sch Sci Rev 40:289 –301.
Miles DB, Dunham AE. 1993. Historical perspectives in ecology
and evolutionary biology: the use of phylogenetic comparative
analyses. Annu Rev Ecol Syst 24:587– 619.
Mittermeier RA, Tattersall I, Konstat WR, Meyers DM, Mast RB.
1994. Lemurs of Madagascar. Washington, DC: Conservation
International.
Moller AP, Birkhead TR. 1992. A pairwise comparative method as
illustrated by copulation frequency in birds. Am Nat 139:644 –
656.
Mosimann JE. 1970. Size allometry: size and shape variables
with characterizations of the lognormal and generalized
gamma distributions. J Am Stat Assoc 65:930 –945.
Mosimann JE, James FC. 1979. New statistical methods for allometry with application to Florida red-winged blackbirds. Evolution 33:444 – 459.
Moss ML. 1968. Functional cranial analysis of mammalian mandibular ramal morphology. Acta Anat (Basel) 71:423– 447.
Muskin A. 1984. Field notes and geographic distribution of Callithrix aurita in eastern Brazil. Am J Primatol 7:377–380.
Nash LT. 1986. Dietary, behavioral, and morphological aspects of
gummivory in primates. Yrbk Phys Anthropol 29:113–137.
Natori M, Shigehara N. 1992. Interspecific differences in lower
dentition among eastern-Brazilian marmosets. J Mammal 73:
668 – 671.
Pariente GF. 1975. Lumière et rythme d’activité de Phaner furcifer (Prosimien nocturne de Madagascar) dans son milieu naturel. J Physiol (Paris) 70:637– 647.
Petter JJ, Schilling A, Pariente G. 1971. Observations écoéthologiques sur deux lémuriens malgaches nocturens: Phaner
furcifer et Microcebus coquereli. Terre Vie 25:287–327.
Petter JJ, Albignac R, Rumpler Y. 1977. Mammifères Lémuriens
(Primates Prosimiens). Faune Madagascar 44:1–513.
Purvis A, Bronham L. 1997. Estimating the transition/transversion ratio from independent pairwise comparisons with an assumed phylogeny. J Mol Evol 44:112–119.
Ramirez MF, Freese CH, Revella C. 1977. Feeding ecology of the
pygmy marmoset, Cebuella pygmaea, in northeastern Peru. In:
Kleiman D, editor. The biology and conservation of the Callitrichidae. Washington, DC: Smithsonian Institution Press.
p 91–104.
Ramsey RW, Street SF. 1940. The isometric length tension diagram of isolated skeletal muscle fibers in the frog. J Cell Comp
Physiol 15:11–34.
Ravosa MJ. 1990. Functional assessment of subfamily variation
in maxillomandibular morphology among Old World monkeys.
Am J Phys Anthropol 82:199 –212.
Ravosa MJ. 1991. Structural allometry of the prosimian mandibular corpus and symphysis. J Hum Evol 20:3–20.
Ravosa MJ. 1996a. Mandibular form and function in North American and European Adapidae and Omomyidae. J Morphol 229:
171–190.
169
Ravosa MJ. 1996b. Jaw scaling and biomechanics in fossil taxa. J
Hum Evol 30:159 –160.
Ravosa MJ, Hylander WL. 1994. Function and fusion of the
mandibular symphysis in primates: stiffness or strength? In:
Fleagle JG, Kay RF, editors. Anthropoid origins. New York:
Plenum Press. p 447– 468.
Ravosa MJ, Simons EL. 1994. Mandibular growth and function in
Archaeolemur. Am J Phys Anthropol 95:63–76.
Ravosa MJ, Vinyard CJ, Gagnon M, Islam SA. 2000. Evolution of
anthropoid jaw loading and kinematic patterns. Am J Phys
Anthropol 112:493–516.
Rice WR. 1989. Analyzing tables of statistical tests. Evolution
43:223–225.
Rosenberger AL. 1978. Loss of incisor enamel in marmosets. J
Mammal 59:207–208.
Rosenberger AL. 1992. Evolution of feeding niches in New World
monkeys. Am J Phys Anthropol 88:525–562.
Ross CF. 2001. In vivo function of the craniofacial haft: the
interorbital “pillar.” Am J Phys Anthropol 116:108 –139.
Ruff C. 1988. Himdlimb articular surface allometry in Hominoidea and Macaca, with comparisons to diaphyseal scaling. J
Hum Evol 17:687–714.
Rylands AB. 1981. Preliminary field observations on the marmoset, Callithrix humeralifer intermedius (Hershkovitz, 1977) at
Dardanelos, Rio Aripuana, Mato Grosso. Primates 22:46 –59.
Rylands AB. 1984. Exudate-eating and tree-gouging by marmosets (Callitrichidae, Primates). In: Chadwick AC, Sutton SL,
editors. Tropical rain forest: the Leeds Symposium. Leeds:
Leeds Philosophical and Literary Society. p 155–168.
Siegal S, Castellan NJ. 1988. Nonparametric statistics for the
behavioral sciences. New York: McGraw-Hill.
Smith RJ. 1978. Mandibular biomechanics and temporomandibular joint function in primates. Am J Phys Anthropol 49:341–
350.
Smith RJ. 1983. The mandibular corpus of female primates: taxonomic, dietary, and allometric correlates of interspecific variations in size and shape. Am J Phys Anthropol 61:315–330.
Smith RJ. 1984. Comparative functional morphology of maximum mandibular opening (gape) in primates. In: Chivers DJ,
Wood BA, Bilsborough A, editors. Food acquisition and processing in primates. New York: Plenum Press. p 231–255.
Smith RJ. 1993. Categories of allometry: body size versus biomechanics. J Hum Evol 24:173–182.
Smith RJ, Jungers WL. 1997. Body mass in comparative primatology. J Hum Evol 32:523–559.
Smith RJ, Petersen CE, Gipe DP. 1983. Size and shape of the
mandibular condyle in primates. J Morphol 177:59 – 68.
Soini P. 1982. Ecology and population dynamics of the pygmy
marmoset, Cebuella pygmaea. Folia Primatol (Basel) 39:1–21.
Spencer MA. 1999. Constraints on masticatory system evolution
in anthropoid primates. Am J Phys Anthropol 108:483–506.
Spencer MA, Spencer GS. 1995. Technical note: video-based
three-dimensional morphometrics. Am J Phys Anthropol 96:
443– 453.
Stevenson MF, Rylands AB. 1988. The marmosets, genus Callithrix. In: Mittermeier RA, Rylands AB, Combra-Filho AF,
Fonseca GAB, editors. Ecology and behavior of neotropical primates. Volume 2. Washington, DC: World Wildlife Fund.
p 131–222.
Sussman RW, Kinzey WG. 1984. The ecological role of the Callitrichidae: a review. Am J Phys Anthropol 64:419 – 449.
Szalay FS, Delson E. 1979. Evolutionary history of the primates.
New York: Academic Press.
Szalay FS, Seligsohn D. 1977. Why did the strepsirhine tooth
comb evolve? Folia Primatol (Basel) 27:75– 82.
Turnbull WD. 1970. Mammalian masticatory apparatus. Fieldiana Geol 18:1–356.
Vinyard CJ. 1999. Temporomandibular joint morphology and
function in strepsirhine and Eocene primates. Ph.D. dissertation. Northwestern University.
Vinyard CJ, Wall CE, Williams SH, Schmitt D, Hylander WL.
2001. A preliminary report on the jaw mechanics during tree
170
C.J. VINYARD ET AL.
gouging in common marmosets (Callithrix jacchus). In: Brooks
A, editor. Dental morphology 2001: proceedings of the 12th
International Symposium on Dental Morphology. Sheffield:
Sheffield Academic Press. p 283–297.
Wall CE. 1999. A model of temporomandibular joint function in
anthropoid primates based on condylar movements during
mastication. Am J Phys Anthropol 109:67– 88.
Ward SC, Molnar S. 1980. Experimental stress analysis of topographic diversity in early hominid gnathic morphology. Am J
Phys Anthropol 53:383–396.
Williams SH, Wall CE. 1999. Morphological correlates of gummivory in the skull of prosimian primates. Am J Phys Anthropol [Suppl] 28:278.
Williams SH, Vinyard CJ, Wall CE. 2000. The mechanics of
tree-gouging in Callithrix jacchus. Am J Phys Anthropol
[Suppl] 30:322.
Wolff-Exalto EA. 1951. On differences in the lower jaw of animalivorous and herbivorous mammals, I. Proc Kon Ned Akad
Wetenschapen Amster Ser C 54:237–246.
Yoder AD. 1997. Back to the future: a synthesis of strepsirhine
systematics. Evol Anthropol 6:11–22.
Zar JH. 1999. Biostatistical analysis. Upper Saddle River, NJ:
Prentice Hall.
Zingeser MR. 1973. Dentition of Brachyteles arachnoides with
reference to Alouattine and Atelinine affinities. Folia Primatol
(Basel) 20:351–390.
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