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Comparative microcomputed tomography and histological study of maxillary pneumatization in four species of new world monkeys The perinatal period.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 144:392–410 (2011)
Comparative Microcomputed Tomography and
Histological Study of Maxillary Pneumatization in Four
Species of New World Monkeys: The Perinatal Period
Timothy D. Smith,1,2* James B. Rossie,3 Gregory M. Cooper,4 Robin M. Schmieg,1
Christopher J. Bonar,5 Mark P. Mooney,2,6 and Michael I. Siegel2
1
School of Physical Therapy, Slippery Rock University, Slippery Rock, PA
Department of Anthropology, University of Pittsburgh, Pittsburgh, PA
3
Department of Anthropology, SUNY Stony Brook, Stony Brook, NY
4
Department of Surgery, Oral Biology, and Bioengineering, University of Pittsburgh, Pittsburgh, PA
5
Cleveland Metroparks Zoo, Cleveland, OH
6
Department of Oral Biology, University of Pittsburgh, Pittsburgh, PA
2
KEY WORDS
craniofacial; nasal cavity; paranasal; pneumatization; primate
ABSTRACT
In anthropoid primates, it has been
hypothesized that the magnitude of maxillary sinus
growth is influenced by adjacent dental and soft tissue
matrices. Relatively, little comparative evidence exists for
the perinatal period when secondary pneumatization is at
its earliest stages in some primates. Here, dental and
midfacial variables were studied in a perinatal sample of
four anthropoid primates, including three callitrichines
(Leontopithecus, Saguinus, and Callithrix) and Saimiri
boliviensis. In the latter species, the maxillary recess (the
ontogenetic precursor to a ‘‘true’’ maxillary sinus) does
not undergo secondary pneumatization. Using histological
methods and micro-computed tomography, midfacial and
dental dimensions and radiographic hydroxyapatite density of tooth cusps were measured. The distribution of
osteoclasts and osteoblasts was also documented. Krus-
kal–Wallis’s one-way analysis of variance tests indicates
significant (P < 0.05) differences among groups for dental
and midfacial measurements. In particular, the posterior
maxillary dentition is relatively larger and more mineralized in Saimiri compared to the callitrichines. At posterior dental levels, Saimiri has the lowest palatonasal
index [interdental (palatal) width/width of the nasal cavity] and highest bizygomatic–interorbital index. Distribution of osteoclasts indicates that the inferomedial surfaces
of the orbits are resorptive in perinatal Saimiri, whereas,
in all callitrichines, these surfaces are depository. Taken
together, these findings suggest that pneumatization in
Saimiri is suppressed by an inward growth trajectory of
the orbits, relatively large posterior dentition, and a correspondingly compressed nasal region. Am J Phys
Anthropol 144:392–410, 2011. V 2010 Wiley-Liss, Inc.
Paranasal sinuses are air-filled mucosal evaginations
into the facial skeleton that emanate from smaller
‘‘recesses’’ of the developing nasal fossa (Witmer, 1999;
Maier, 2000; Rossie, 2006). Paranasal sinus expansion,
also termed secondary pneumatization, may provide a
growth mechanism for resolving spatial shifts among
skeletal elements of the nasal capsule, orbit, and dentition (Proetz, 1922; Shea, 1985; Enlow and Hans, 1996;
Rossie, 2003; Zollikofer and Weissman, 2008). In this
view, variations in the nature of sinus expansion are
construed primarily to result from specific craniofacial
growth patterns; other functions that have been offered
to explain sinus shape and size in adult mammals (e.g.,
those related to climate or mastication) would be secondary adaptations (Enlow and Hans, 1996).
At present, our knowledge of the relationship of the
developing sinus to adjacent structures relies disproportionately on evidence from humans and a few nonhuman
primates. For example, clinical and comparative evidence demonstrates that the bony wall of the maxillary
sinus surrounds tooth crypts during growth and (later)
the root tips, such that portions of the teeth create
bulges into the sinus cavity (Schaeffer, 1920; Koppe and
Nagai, 1999; Rossie, 2006). It is difficult to ascertain the
nature of association between the dentition or palatal
form and the final shape of the maxillary sinus, despite
their close proximity in many primates (Koppe and
Nagai, 1999; Swindler, 1999). Two factors make this
determination difficult. First, because the interrelationship between sinus and dental/osseous morphology
changes throughout development, an understanding of
the earliest phases of sinus formation is essential; that
is, when the sinuses first pneumatize beyond the limits
of the nasal capsule. Early development of the most precocious paranasal space, the maxillary sinus, is well
documented in humans as an event beginning in the second trimester [(Koppe et al., 1994; Smith et al., 1997;
and see Sperber (2000)], whereas it is poorly understood
across nonhuman primates. Second, a comparative primate perspective at early stages of development has
C 2010
V
WILEY-LISS, INC.
C
Grant sponsor: National Science Foundation; Grant numbers:
BCS-0820751, BCS-0610514.
Present address of Christopher J. Bonar: Dallas World Aquarium, 1801 N. Griffin St., Dallas, Texas 75202, USA.
*Correspondence to: Timothy D. Smith, School of Physical
Therapy, Slippery Rock University, Slippery Rock, PA 16057.
E-mail: timothy.smith@sru.edu
Received 1 May 2010; accepted 10 September 2010
DOI 10.1002/ajpa.21421
Published online 29 November 2010 in Wiley Online Library
(wileyonlinelibrary.com).
393
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
been elusive, in part, because generating samples of subadult primates is relatively challenging. An even more
challenging issue is the apparent ontogenetic differences
in the timing of pneumatic expansion among primates
that form a maxillary sinus (Rossie, 2006; Smith et al.,
2010).
Recently, several studies have begun to address the
paucity of ontogenetic information. It has been hypothesized that the size and position of the maxillary dentition is critical factor influencing the extent of pneumatic
expansion of the maxillary recess (Smith et al., 2005,
2010; Rossie, 2006). Microanatomical evidence on several
species of callitrichines suggests that where the skeletal
units bordering the deciduous premolars and developing
maxillary sinus form a shared bony lamina, lateral
expansion of this paranasal space is inhibited locally by
the dental follicle (Smith et al., 2005). In ontogenetic
samples of New World monkeys, relative dental size
and the proximity of the alveolar and orbital skeletal
structures of the maxilla appear to relate inversely
to the extent of pneumatization (Rossie, 2006; Smith
et al., 2010). Left unclear is the relative importance
of each of these neighboring structures and spaces, a
question that may be best answered using a comparative
sample.
Previously, we have emphasized the potential value of
New World primate samples as natural experiments to
understand pneumatization (Rossie, 2006; Smith et al.,
2010). The specific aims of this study are to test hypotheses generated by bone-cell distribution along the maxillary sinus walls in callitrichines (Smith et al., 2005) and
by an ontogenetic comparison of the maxillary recess of
Saimiri to the maxillary sinus of Saguinus and Cebuella
(Smith et al., 2010). In these studies, we hypothesized
that large relative size of the posterior maxillary dentition, a high degree of orbital approximation, and low-palatonasal indices [interdental (palatal) width/width of the
nasal cavity] each act to constrain pneumatization from
the maxillary recess in Saimiri. Here, to test these
hypotheses, we compare these measures among four species with differing degrees of pneumatic expansion
within the maxilla, including one species that does not
form a maxillary sinus postnatally.
MATERIALS AND METHODS
Sample
We studied four species of New World monkeys that
differ in postnasal paranasal morphology. All species
form a maxillary ‘‘recess,’’ a space formed by prenatal
growth and folding of the cartilaginous nasal capsule
(‘‘primary pneumatization’’). These species differ in the
extent of secondary pneumatization of this recess, a process by which the mucosa-lined space invades the adjacent maxilla after breakdown of the cartilaginous capsule. In three of these species, Saguinus oedipus, Leontopithecus rosalia, and Callithrix jacchus, a maxillary
sinus has been described in adult specimens by numerous authors (e.g., Nishimura et al., 2005; Rossie, 2006;
Smith et al., 2010). In the fourth, Saimiri boliviensis, no
secondary pneumatization occurs (Smith et al., 2010), as
also reported for S. sciureus Rossie, 2003, 2006; Nishimura et al., 2005). Previously, we have distinguished
between ‘‘true’’ paranasal sinuses (the final product of
secondary pneumatization) and paranasal recesses that
persist in adults in the absence of secondary pneumati-
TABLE 1. Age and sexes of the sample under study
Species
n (sex)
Age range (d)
Saguinus oedipus
5 (2 m, 2 f, 1 u)
Leontopithecus rosalia
Callithrix jacchus
6 (1 m; 5 f)
5 (2 m, 2 f, 1 u)
Saimiri boliviensis
6 (5 m, 1 u)
0 (stillborn or died
on P0)
0–9
0 (stillborn or died
perinatally)
0–10
d, days; f, female; m, male; u, unknown sex.
zation (Rossie, 2006; Smith et al., 2010). Thus, according
to our terminology, Saimiri lacks a maxillary sinus.
Twenty-two specimens were studied (Table 1). All
specimens were acquired from cadaveric remains preserved in 10% formalin. This opportunistic sample
included animals that were stillborn or died within 10
days of birth in captivity at the New England Primate
Center, the University of South Alabama Primate
Research Center, the Wisconson National Primate
Research Center, or the Cleveland Metroparks zoo.
When possible, both males and females of each species
were acquired. However, only male perinatal Saimiri
(and one of unknown sex) were available for study. Becasue adults of the genus Saimiri are described to have
only minimal dimorphism (Corner and Richtsmeier,
1992), it is not expected that Saimiri boliviensis is
dimorphic at birth.
The specimens are not all assumed to be neonatal in
stage of somatic maturity and likely represent a mix of
premature and early postnatal stages (thus, these are
referred to as a ‘‘perinatal’’ sample). Perinatal specimens
of known age were either stillborn or died from ages P0
to P10 (Table 1). Although facial and dental development
and growth are presumably rapid in the interval of ages
that are available for study, this sample was considered
a relatively cohesive group for two reasons. First, endochondral ossification of the lateral nasal wall is underway in all specimens. In all species, only remnants of
cartilage are observed along the lateral borders of the
nasal fossa, including the maxillary recess [see Smith et
al. (2005, 2010)]. Thus, all species have passed the stage
in which the ‘‘fetal template’’ of paranasal morphology
(i.e., the stage when cartilage forms continuous boundaries around the lateral nasal wall) is apparent [see
Smith et al. (2008)]. Second, the samples appeared to be
relatively consistent in head and midfacial size within
each species. Regarding upper limits in the age range,
the specimens of oldest known age (9-day-old Leontopithecus and 10-day-old Saimiri) were within, not at the
upper limit, the overall range in cranial or palatal
length.
Microcomputed tomography and
histological methods
Sixteen of the perinatal specimens (four of each species) were scanned using microcomputed tomography
(micro–CT; 19-lm voxel size; VivaCT40 scanner, Scanco
Medical, USA). The scans were used to generate threedimensional reconstructions. The threshold for reconstructions was set at 200 dpi, a level selected based in
our ability to detect thin bones such as the turbinals or
individual septa that bordered the paranasal spaces. Radiographic hydroxyapatite (HA) density was measured to
assess the rate of mineralization of the dentition from
American Journal of Physical Anthropology
394
T.D. SMITH ET AL.
TABLE 2. Distribution of osteoclasts and osteoblasts along surfaces of the ethmoid and maxillary bones
Genus/dental level
Saguinus
Dp2
Dp3
Dp4
M1
Leontopithecus
Dp2
Dp3
Dp4
M1
Species/level
Callithrix
Dp2
Dp3
Dp4
M1
Saimiri
Dp2
Dp3
Dp4
M1
Orbit medial
Orbit floor
Inferomedial Orbit
Medial alveolar wall
1
Variable
2
6b or NA
1
1
1
1
1
1
1
1
Variablea
6b
Variable
6b
1
1
Variable
2
1
1
1
NA
1
1
1
1
1c
Variable
2d
NA
1
1
1c
1 or NA
1
1
1c
1
1
1
1
1
1
Variable
Variable
NA
2d
2
2
2
1
Variable
2d
2 or NA
1
2
2
2
6b
6b
2d
2
a
Predominantly osteoblasts, osteoclasts, or a mix of bone cells in different specimens.
In the same individual, there were both osteoclastic and osteoblastic foci in this region.
Limited numbers of osteoclasts seen in some specimens.
d
Limited groups of osteoblasts seen in some specimens. 1, osteoblasts; 2, OC, osteoclasts; NA, not applicable (e.g., ethmoid is cartilaginous or there is no maxillary bone at this level).
b
c
the anterior to posterior limits of the maxillary tooth
row. The threshold for measurements was set at 200 dpi.
Density was only measured from deciduous dentition,
because M1 is poorly mineralized in all species except
Saimiri. HA density was obtained for volumetric segments of enamel in slices extending for about 0.48 mm
(25 slices). For premolars with multiple cusps, the buccomesial cusp was selected in all specimens. HA density is
ultimately determined by calibrating the VivaCT using a
phantom that has samples of known concentrations of
HA. Then optical density (radiodensity) is measured and
interpreted as mg HA/cc (Usas et al., 2009).
After micro-CT scanning, the specimens were dissected
and processed for paraffin embedding. The histological
sample also included specimens previously sectioned for
studies of other nasal structures [see Smith et al. (2003)
and Dennis et al. (2004) for details]. Before embedding,
cranial length (prosthion-inion) and palatal length (prosthion–posterior mid-palatal point) were measured with
digital calipers to the nearest 0.01 mm. In some specimens, damage during necropsy prevented acquisition of
these measurements. However, these samples were still
useful for calculation of palatal and nasal breadth indices (see below). All paraffin-embedded heads used in this
study were serially sectioned at 10 lm and stained for
histomorphometric analysis using ImageJ software
(NIH). For each species, three specimens were sectioned
in the coronal plane. In one specimen of each species,
half the head was sectioned coronally, while the contralateral half was sectioned in the sagittal plane. At least
every 10th section was mounted on glass slides with serial numbers and stained with hematoxylin-eosin and
Gomori trichrome procedures. Intervening sections were
saved for future histochemical and immunohistochemical
analysis.
Using a Leica DMLB microscope, each stained section
was examined at magnifications from 325 to 3100 to
American Journal of Physical Anthropology
assess position of the sinus or recess and adjacent structures such as dental sacs. After the first section containing the deciduous canine and the last section containing
M1 were identified, anteroposterior ‘‘start’’ and ‘‘stop’’
points of all intervening dental sacs and the sinus or
recess were noted to determine their spatial relationship.
At higher magnification (3200–3630), the distribution of
osteoblasts and osteoclasts was observed along osseous
contours of the medial and inferior orbit and along the
medial side of the alveolar socket for each tooth from
dp2 to M1. For each specimen, three sections in the midlevel of each dental sac were used to record whether
these surfaces were predominantly lined with osteoblasts
and thus showed evidence for bone deposition or lined
with multinucleate osteoclasts and thus interpreted as
resorptive surfaces. Also noted were surfaces with mixed
distribution of osteoblasts and osteoclasts or surfaces
that were devoid of bone cells. Based on all specimens of
each species, Table 2 lists the bone cell distribution by
species and region, with intraspecific variation noted.
Representative sections that showed the characteristic
distribution of bone cells were selected for graphical
representation.
Histomorphometrics
Most of the Saguinus and Saimiri sample was previously analyzed in an ontogenetic study of some palatal,
nasal, and dental variables (Smith et al., 2010). Some of
these data are included in this comparative analysis.
However, we have expanded the analysis to include additional dental levels, more species, more variables, and
one additional specimen of Saguinus, prepared specifically for this study. For most variables, data were
obtained at mid-cross-sectional levels for each of the
maxillary tooth follicles from the deciduous canine to the
first permanent molar (M1). Palatonasal indices (see
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
395
gin of alveolar bone was often indistinct in perinatal animals, alternative landmarks were used: the medial margin
of the right and left dental follicles. As per Rossie (2006),
nasal width was measured as the distance between the
right and left sides of lateral nasal wall at the base of the
nasal fossa (this corresponds to the wall of the inferior meatus at the level of the last deciduous premolar). The distance between right and left sides was measured as palatal width. The index was then calculated as interdental
width/nasal width. In specimens where only half of the
face was sectioned in the coronal plane, the ratio was calculated by measuring one-half of the distances from the
dental sac or lateral limit of the nasal fossa to the midline
(using the center of the palate as the midline). Two additional indices were calculated for this study:
1. Bizygomaticonasal indices (Fig. 1b) were calculated
as maximum bizygomatic width/nasal width. This
index assesses the overlap of nasal cavity width relative to facial width. In specimens where only half
of the face was sectioned in the coronal plane, this
ratio was calculated by measuring one-half of the
distances from the maximum lateral limit of the zygoma or lateral limit of the nasal fossa to the midline (center of the palate).
2. Bizygomatic–interorbital indices (Fig. 1c) were calculated as maximum bizygomatic width/minimum
interorbital width. This index assesses relative
interorbital width. It is a measurement relating to
the extent of orbital approximation. In specimens
where only half of the face was sectioned in the coronal plane, this ratio was calculated by measuring
one-half of the distances from the maximum lateral
limit of the zygoma or lateral limit of the nasal
fossa to the midline (center of the palate).
Fig. 1. Indices of midfacial dimensions used in this study.
BZW, bizygomatic width; IOW, interorbital width; NW, nasal
width; PW, palatal width.
below) were only measured from the levels of the first
deciduous premolar (dp2) to M1, because the maxillary
sinus/recess is posterior to the mid-level of the deciduous
or adult canine in each of these species (Smith et al.,
2005, 2010). Bizygomatic and interorbital distances (see
below) were only measured at the level of the last deciduous premolar (dp4) and M1, because the zygoma is not
in the plane of section anterior to dp4 in all species.
To acquire data from the histological sample, each
stained section ranging from the deciduous canine to M1
was photographed using a Leica DMLB microscope and
Cat-Eye digital camera. Measurements were then taken
from digital micrographs of histological sections using
ImageJ software (NIH). Palatonasal index (Fig. 1a),
which measures the proportional relationship between
palatal and nasal cavity dimensions, was modified from
Rossie (2006). Rossie measured palatal width as the distance between right and left medial alveolar margins of
the maxilla (2006, see Fig. 42). Because the medial mar-
Using ImageJ software, dental sac volumes were
measured for all maxillary teeth (from deciduous canine
to M1) on the right side of the nasal fossa, except in two
specimens where damage to the follicles prevented measurements. Among specimens in which right and left
sides were both well-preserved for measurement, asymmetry was not biased toward one side (in about half of
the specimens, the right dental sacs were larger and in
the other half the left sacs were larger). Therefore, the
left side was used for analysis in the two specimens where
the right side was damaged. Volumes were acquired by
tracing the cross-sectional area of the dental sac as estimated by the outer edge of the outer enamel epithelium.
Once all sections containing a cross-section of the tooth
were measured, the cross-sectional areas in millimeter
square were multiplied by the distance between sections
for a segmental volume of the tooth. This was repeated for
each section of the tooth up to the penultimate section
(the last section containing the tooth was regarded as the
end). Then, all segmental volumes were summed to obtain
total volume of the tooth. The cube root of these tooth volumes was divided by palatal and cranial lengths to obtain
relative size of the tooth follicles.
Statistical analyses
SPSS 15.0 (SPSS) was used to analyze the data. Data
were compared between groups using a Kruskal–Wallis
one-way analysis of variance test. All differences were
considered significant at P 0.05. Differences between
species were then assessed using a post hoc test for mulAmerican Journal of Physical Anthropology
396
T.D. SMITH ET AL.
Fig. 2. Schematic graph illustrating the spatial overlap of
the maxillary sinus or recess (gold) and the dental follicles in
the four genera. The anteroposterior space is indicated from left
to right, with 0% indicating the sectional level of the first histological section in which the deciduous canine appears, and 100%
indicating the last section in which M1 appears. The graph
illustrates an average of all specimens for each species. The
graph is intended to show anteroposterior overlap only. Note
that superoinferior separation is exaggerated; the sinus sac is
actually more closely adjacent to the dentition, especially at posterior levels. dc, deciduous canine; M1, first permanent molar.
tiple comparisons between treatments (Siegel and Castellan, 1988, p 213), with differences considered different
at P 0.05.
American Journal of Physical Anthropology
Fig. 3. Parasagittal sections at the level of the mucosal lining of the maxillary sinus (ms) in Saguinus (a), Leontopithecus
(b), and Callithrix (c) and the maxillary recess (mr) of Saimiri
(d). Note that the paranasal space intervenes between the orbit
(or) and the anterior maxillary dentition in all species. Even
though orbits appear proportionately large in Saguinus and
Callithrix, the posterior part of the sinus occupies a space that
is relatively uncrowded compared to the other species, due to
relatively smaller premolar follicles. However, in Leontopithecus, the sinus appears to be the most expansive, perhaps due to
proportionately small orbits (Fig. 3b). dc, deciduous canine; dp2,
first deciduous premolar; dp3, second deciduous premolar. Scale
bars, 1 mm. The background in low-magnification images (11a,
c, e, g) was digitally altered, because the lighting was unbalanced; portions of the image containing tissue were not altered.
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
397
Fig. 4. Micro-CT reconstruction showing the facial skeleton of Saguinus (a), Leontopithecus (b), and Callithrix (c) and Saimiri
(d) in the frontal view. Note the proportionally small interorbital distance in Saimiri (d). Also note that the greater degree of frontation of the zygomatic bones (Z) in Saimiri. M, maxilla; F, frontal bone. Scale bars, 1 mm.
RESULTS
Relative position of the maxillary
sinus or recess to dentition
Figure 2 shows the position of the maxillary sinus or
recess, specifically, the mucosal sac, relative to dental
level in the four species of primates. Anteroposterior
space of the deciduous maxillary dentition, from the first
serial histological section containing the deciduous canine to the last section containing M1, establishes the
limits of the space shown in the graph. This figure
graphically depicts the sinus sac above the maxillary
teeth for clarity, whereas the actual position of the mucosal sac is superomedial or medial to the dental follicles
(see below). In all callitrichines, the ostium of the sinus
overlaps dc and dp2, and the enclosed sinus completely
overlaps dp2 and dp3 in anteroposterior extent. The
level of dp4 is partially overlapped in anteroposterior
space, especially in Leontopithecus, where the sac
extends to overlap approximately one-half of this dental
follicle. In contrast, the mucosal sac of the maxillary
recess in Saimiri is restricted to the anteroposterior
space occupied by dp2 and dp3.
Figure 3 depicts parasagittal sections at the level of
the maxillary sinus or recess in the four primate species.
The anterior portion of the sinus in the callitrichines
(Fig. 2a–c) is oriented in a posterior and obliquely inferior direction from its ostium (ostium, not shown, is at
anterior limit) toward dp3. In this respect, this portion
of the sinus is positioned similarly to the entire maxillary recess in Saimiri (Figs. 2 and 3d). At the level of anterior part of dp3, the maxillary sinus of all callitrichines
changes orientation to follow the palatal plane (Figs. 2
and 3a–c).
Interrelationship of the orbit, nasal
fossa, and dentition in the tamarins,
marmoset, and squirrel monkey
Micro-CT reconstructions of skulls of the four primate
species, in anterior view, are shown in Figure 4. This
view reveals differing interorbital proportions among
species, appearing to be relatively wide in tamarins in
relation to the overall facial breadth (Fig. 4a,b), proportionately more narrow in Callithrix (Fig. 4c) and narrowest in Saimiri (Fig. 4d). Figure 5, also in an anterior
view, shows the same specimens cross-sectioned at the
level of dp2. At this level, the osseous maxillary sinus/
recess has a wide opening into the middle meatus in all
species. The floor of the maxillary recess in Saimiri is
positioned at same plane as the orbital floor (Fig. 5d),
whereas it extends more inferiorly in callitrichines,
nearly reaching the same horizontal plane as the floor of
the nasal fossa in Leontopithecus (Fig. 5b). Figure 6
shows the same specimens cross-sectioned at the level of
dp3. At the level, the sinus cavities are proportionately
American Journal of Physical Anthropology
Fig. 5. Micro-CT reconstruction showing the facial skeleton of Saguinus (a), Leontopithecus (b), Callithrix (c), and Saimiri (d) in the
frontal view cut at the level of the first deciduous premolar (dp2). The position of the maxillary sinus or recess (white arrows) is shown near
its ostium. The inferior meatus is indicated (black arrows). The sinus is most inferiorly expanded in Leontopithecus. Scale bars, 1 mm.
Fig. 6. Micro-CT reconstruction showing the facial skeleton of Saguinus (a), Leontopithecus (b), Callithrix (c), and Saimiri (d)
in the frontal view cut at the level of the second deciduous premolar (dp3). The position of the maxillary sinus or recess (white
arrows) is shown. The inferior meatus is indicated (black arrows). The sinus is most inferiorly expanded in Leontopithecus. The
maxillary recess or Saimiri is mostly above horizontal plane of dp3 and above the floor of the nasal fossa (see inferior meatus). The
sinus in Saguinus and Callithrix is parallel to the floor of the inferior meatus. Scale bars, 1 mm.
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
399
Figures 6 and 7 emphasize differing orbital proportions and interorbital dimensions at the level of dp3.
Qualitatively, the orbits appear proportionately smallest,
and the interorbital breadth is proportionately greatest
in Leontopithecus (Figs. 6b and 7a). Orbits are proportionately larger, and the interorbital breadth is proportionately smaller in Callithrix (Figs. 6c and 7b) and Saimiri (Figs. 6d and 7c). However, relative to biorbital
breadth, the bialveolar breadth appears greater in callitrichines than Saimiri (Figs. 6 and 7).
Figure 8 shows the relationship of the orbits and nasal
cavity in the four species at a horizontal plane approximately mid-way through the orbit. This view confirms
visual impressions from the anterior view (see Fig. 4)
showing that the nasal cavity is proportionally widest in
the tamarins (Fig. 8a,b) compared to Callithrix (Fig. 8c)
and Saimiri (Fig. 8d). The position of the orbits relative
to the nasal cavity and orbital orientation also differs
among species. In Callithrix (Fig. 8c) and especially
Saimiri (Fig. 8d), the orbits encroach on the posterior
nasal cavity to a greater degree than in the tamarins
(Fig. 8a,b). However, the orientation of the orbital cones
is more lateral in all callitrichines (Fig. 8a–c) compared
to Saimiri (Fig. 8d). Figure 9 shows a horizontal section
through the perinatal skulls of Saguinus (Fig. 9a) and
Saimiri (Fig. 9b) closer to the floor of the orbit. Here,
the floor of the cavity for the maxillary sinus or recess is
shown medial to the orbit. The relatively large orbit of
Saimiri compresses the paranasal space posteriorly. As a
result, the maxillary recess of Saimiri is constricted posteriorly and oriented obliquely in a medial direction from
its anterior to posterior limit (Fig. 9b). In Saguinus, the
maxillary sinus is more nearly parasagittal in its orientation (Fig. 9a).
Comparative development of the maxillary
dentition and alveolar bone
Fig. 7. Micro-CT reconstruction showing the facial skeleton of
Leontopithecus (a), Callithrix (b), and Saimiri (c) in the posterior
view cut at the level of the second deciduous premolar (dp3) and
tilted inferiorly. The position of the maxillary sinus or recess
(white arrows) is shown (in Saimiri, this level is just posterior to
the recess, but its position is indicated). This view emphasizes the
greater degree of encroachment of the orbits on the nasal fossa
and potential paranasal space. Scale bars, 1 mm.
most expanded in tamarins (Fig. 6a,b). Inferiorly, the
sinus cavity reaches the same plane as the floor of the
nasal fossa in all callitrichines (Fig. 6a–c). In Saimiri,
the maxillary recess is positionally consistent with the
sinuses of the callitrichines at this level, but is less
expanded inferiorly toward the level of the nasal fossa
floor (Fig. 6d).
Micro-CT reconstructions revealed that, in all species,
the most anterior maxillary teeth are partially erupted
through alveolar bone, whereas posterior maxillary
teeth, especially dp4 and M1, are positioned more deeply
within alveolar crypts or had no detectable bone immediately surrounding them (see Fig. 10). The cusps of the
deciduous canine and dp2, in particular, are partially
erupted in all species (Figs. 5 and 7).
Across the entire maxillary tooth row, deciduous eruption was most advanced in Callithrix (Figs. 5c, 6c, and
7b). The extent of ossification of the posterior portion of
the maxillary bone appears to be more progressive in
Leontopithecus and Saimiri (Fig. 10b,d) compared to
Saguinus and Callithrix (Fig. 10a,c). Micro-CT reconstructions indicate that the maxillary teeth are least
mineralized in Saguinus in that the cusps of dp3 and
dp4 are not united, and only a single cusp of M1 is mineralized (Fig. 10a). The other species show a greater
degree of mineralization between cusps of dp3 and dp4.
Saimiri is remarkable for the extent of mineralization of
M1, which has two or three cusps partially mineralized
(Fig. 10d).
Although the threshold selected for micro-CT reconstructions may not permit detection of some poorly mineralized bone, histological preparations support these
observations. Figure 11 shows sections through the parasagittal plane that transect all maxillary tooth follicles.
These trichrome-stained preparations clearly illustrate
American Journal of Physical Anthropology
400
T.D. SMITH ET AL.
Fig. 8. Micro-CT reconstruction showing the facial skeleton of Saguinus (a), Leontopithecus (b), Callithrix (c), and Saimiri (d)
in the superior view cut approximately at the superoinferior mid-level of the orbit. Note that the inferior contour of the orbit, from
the maxilla to the zygomatic bones, is oriented more laterally in the callitrichines compared to Saimiri. This suggests a greater
degree of convergence of the orbit in Saimiri. Scale bars, 1 mm.
that maxillary bone barely extends to the level of dp4 in
Saguinus and Callithrix (Fig. 11a,b,e,f). In Leontopithecus and Saimiri, alveolar bone is beginning to surround
the anterior extent of M1 (Fig. 11c,d,g,h).
Distribution of osteoblasts and osteoclasts
along orbital, nasal, and alveolar surfaces
of the maxillary bone and orbital surface of the
ethmoid bone
At all dental levels, the orbital surface of the maxilla
is lined with rows of osteoblasts in all callitrichines (Fig.
12a–e), except for local areas of resorption associated
with the infraorbital neurovascular bundle (Table 2). In
Saimiri, in contrast, the orbital surface of the maxilla is
lined with osteoblasts at the level and dp2 and, to some
extent, at dp3 (Table 2). However, at dp4 and M1 levels,
the orbital surface of the maxilla has scattered osteoclasts and Howship’s lacunae (Fig. 12f,g and Table 2).
The outer (orbital) surface of the nasal fossa is formed
by the maxillary bone, inferomedially, and more superiorly by the orbital surface of the ethmoid lateral plate.
In all species, a small extent of the ethmoid lateral plate
is still cartilaginous or is ossifying. Inferomedially, the
orbital surface of the lateral nasal wall is lined with
American Journal of Physical Anthropology
osteoblasts in all callitrichines (Fig. 12a and Table 2). In
Saimiri, this region is lined with osteoblasts at dp2, but
has mostly osteoclasts and Howship’s lacunae at more
posterior levels (Fig. 12f and Table 2). The medial wall
of the orbit is formed by the ethmoid lateral plate (anteriorly) or mesethmoid alone. In Saimiri, the medial orbit
was composed of only the mesethmoid at the M1 level;
at dp4 level, the lateral ethmoid is reduced. In most
specimens of Callithrix and Saguinus, the medial orbit
is composed of mesethmoid alone at M1 level. The
medial orbit is mostly lined with osteoblasts in Leontopithecus and Callithrix, but has more osteoclasts posteriorly in Saguinus (Table 2). In Saimiri, the medial orbit
is only lined with osteoclasts and Howship’s lacunae at
posterior dental levels (Table 2).
Distribution of bone cells along the medial alveolar
margins of maxillary tooth crypts is mostly similar in
Saguinus, Leontopithecus, and Saimiri. Foci of osteoclasts or rows of osteoblasts are observed at all sectional
levels except M1, which has little or no alveolar bone
surrounding it in most specimens. Osteoclasts appear to
frequently occur opposite medial swellings of the dental
follicles. Osteoclasts are scattered along the superior and
lateral margins of alveolar crypts in Saguinus, Leontopithecus, and Callithrix. In Callithrix, the medial alveolar
walls of the deciduous premolars are nearly uniformly
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
Fig. 9. Micro-CT reconstruction showing the facial skeleton
of Saguinus (a) and Saimiri (b) in the superior view cut just
above the level of the floor of the nasal fossa. The position of
the maxillary sinus or recess (white arrows) is shown. The osseous root of the maxilloturbinal, separating the maxillary sinus
or recess from the inferior meatus, is indicated (black arrows).
Note the sinus is roughly parallel to the nasal fossa in Saguinus. The maxillary recess of Saimiri is compressed and more
diverted in a medial direction as it extends posteriorly. Scale
bars, 1 mm.
lined with osteoblasts except at M1 (the maxilla does not
extend to this level). Saimiri is distinct from all callitrichines in having mostly osteoblastic surfaces of bone
along the superior limit of the alveolar crypts (Fig. 12g).
Quantitative results
Kruskal–Wallis tests indicate significant (P \ 0.05)
differences among species for relative dental follicle size
for nearly all comparisons (Table 3). The only exception
is the size of M1 relative to cranial length ratio (P [
0.05). For the ratios of cube root of dental follicle volume
to palatal length, post hoc tests (Table 3) indicate that
these results are mainly driven by the large size of the
dc, dp2, and dp3 in Leontopithecus compared to one or
both of the other callitrichines (but not Saimiri). No significant differences were detected between species in a
post hoc test for dp4. The M1-palatal length ratio is largest in Saimiri; post hoc comparison shows that this measurement is significantly (P \ 0.05) larger in Saimiri
401
than Callithrix. When related to cranial length, cube
root of dental follicle volumes reveals a somewhat different pattern. Post hoc tests indicate significantly (P \
0.05) larger dc, dp2, dp3, and dp4 relative to cranial
length in Leontopithecus compared to Saimiri.
Figure 13 graphically depicts the findings listed in Table 3. Overall, a similar trend in relative dental follicle
size is suggested by all graphs for dc, dp2, and dp3. That
is, Leontopithecus has large dental follicles relative to
palatal or cranial length. Relative to palatal length, the
trend in dental follicle size breaks down posteriorly,
where Saimiri equals or exceeds (M1) Leontopithecus in
relative size. Relative to cranial length, the trend is
markedly different at M1, where Leontopithecus is more
similar in relative M1 size to the other callitrichines.
The change in trend is graphically depicted in Figure 14.
Overall, Figures 13 and 14 indicate that the size of the
dentition in Saimiri is much greater relative to palatal
length than it is for cranial length.
Kruskal–Wallis tests reveal significant (P \ 0.05) differences in HA density of the alveolar bone and the tooth
cusps from dc to dp4 (no comparisons were made of M1,
because the not all species had mineralized cusps in
M1). HA density was greatest in Saimiri for all cusps
and least in Callithrix (Table 3 and Fig. 15). Post hoc
tests show that Saimiri and Callithrix were significantly
different from each other at each tooth level (Table 2).
Kruskal–Wallis tests reveal significant (P \ 0.05) differences in palatonasal indices at dp3, dp4, and M1, but
no significant difference (P [ 0.05) at dp2 (Table 3). Post
hoc tests reveal that Saguinus has a significantly
greater palatonasal index compared to Leontopithecus at
dp3, and Saimiri had a significantly lower palatonasal
index compared to Callithrix at M1. Although few significant differences are detected by the post hoc comparisons, Figure 16 shows certain trends in the palatonasal
indices. Aside from dp2 and M1 levels, Saguinus and
Callithrix have a larger palatonasal index compared to
Leontopithecus and Saimiri. That is, the former had
wider palatal widths relative to nasal width. From dp4
to M1, this ratio became progressively lower in Saimiri
compared to the callitrichines (Table 2 and Fig. 16).
That is, the nasal cavity has greater overlap with the
palate.
Kruskal–Wallis tests reveal significant (P \ 0.05) difference in bizygomaticonasal indices at dp4 and M1 (Table 3). Figure 17 shows the indices at the two levels. At
dp4, Saguinus and Callithrix are seen to overlap in the
range of standard error, whereas Leontopithecus falls
below and Saimiri falls above this range. At M1, Saimiri
and Callithrix have the highest indices. Leontopithecus
and Saguinus have lower indices, with overlapping
ranges. Post hoc tests reveal that Saimiri has a significantly greater bizygomaticonasal index compared to
Leontopithecus at both dp4 and M1 levels. Note that Saimiri and Leontopithecus have a consistent difference at
both dental levels: the former has greater bizygomatic
width relative to nasal width.
Bizygomatic–interorbital indices were highly variable
in all species except Leontopithecus (Table 3). This may
be due to variability in the ethmoid bone in Callithrix,
Saguinus, and Saimiri at dp4 and M1. In these species,
the lateral mass of the ethmoid bone was diminutive
(and absent at M1), whereas the lateral mass is prominent at these dental levels in Leontopithecus. Despite
the variability in most species, Kruskal–Wallis tests
reveal significant (P \ 0.05) difference in bizygomatic–
American Journal of Physical Anthropology
402
T.D. SMITH ET AL.
Fig. 10. Micro-CT reconstruction showing the facial skeleton of Saguinus (a), Leontopithecus (b), Callithrix (c), and Saimiri (d)
in the inferior view, showing the extent of mineralization of the maxillary dentition. The dentition appears most mineralized in Saimiri and Leontopithecus and least mineralized in Saguinus. M1 was most mineralized in Saimiri. Scale bars, 1 mm second deciduous premolar; dp4, third deciduous molar. Scale bars, 1 mm. dc, deciduous canine; dp2, first deciduous premolar; dp3, second deciduous premolar; dp4, third deciduous molar. Scale bars, 1 mm.
interorbital indices at dp4 and M1 (Table 3). At dp4,
Leontopithecus has a low index compared to the other
species, indicating a wide separation between the orbits.
At M1, the bizygomatic–interorbital index of Saimiri
remains highly variable based on standard deviation (Table 3), but is larger than all callitrichines (see Fig. 17).
Post hoc tests reveal that Saimiri has a significantly
greater bizygomatic–interorbital index compared to
Leontopithecus at the M1 level; the same trend is seen
at dp4, though it is not significantly different (Table 3
and Fig. 17).
DISCUSSION
Recent studies have sought a clearer understanding of
the process of pneumatic expansion in terms of growth
(Koppe and Nagai, 1997, 1999; Rossie, 2006) and microanatomical changes in the mucosa and cartilage or osseous boundaries (Witmer, 1997; Smith et al., 2005, 2008).
Evidence on the nature of pneumatization has clear benefits for surgical treatment for pathologies and some congenital disorders of the maxillary dentition and midface,
for instance, regarding remodeling subsequent to dental
extractions (Sarnat, 1997). In addition, examining the
interrelationship of developing paranasal spaces and surrounding structures may explain differing patterns of
pneumatization or the lack of pneumatization among different anthropoids. Thus, a firm developmental understanding informs phylogenetic interpretations (Rossie,
2008).
Evidence that the enlargement of paranasal spaces is
linked closely to growth of specific craniofacial structures is supported by some, but not all, studies (Rae
and Koppe, 2004; Rossie, 2006). That the dentition
obstructs maxillary sinus expansion in a localized manAmerican Journal of Physical Anthropology
ner is suggested by all species in which the sinus and
dentition interface directly (Koppe et al., 1995; Koppe
and Nagai, 1999). However, Rae and Koppe (2004) note
that tooth follicles are ‘‘exposed’’ in the maxillary sinus
floor in some but not all macaque species. In addition,
Koppe et al. (1996) found no clear association between
palatal form and maxillary sinus morphology in orangutans. The scaling of maxillary sinus size relative to
body size also differs among anthropoids (Rae and
Koppe, 2000; Koppe et al., 2005). Based on variability
in scaling, and lack of association with specific midfacial morphologies, Koppe and colleagues (Koppe and
Nagai, 1999; Koppe et al., 1999) doubt that pneumatic
expansion can be solely explained by an architectural
or structural theory.
The structural hypothesis and
constraint of pneumatization
Recently, we have suggested that valid tests of structural hypotheses may require examination of earlier
stages of ontogeny (Smith et al., 2010). The hypothesis
that sinuses primarily have an architectural or structural role as opposed to a physiological function has
been articulated by numerous authors, but not always
with the same precise meaning (e.g., Proetz, 1922; Weidenreich, 1924; Moss and Young, 1960; Preuschoft et al.,
2002). Among a list of numerous functions, the hypotheses that pneumatic spaces, either serve to maximize
strength of bones with minimal materials or are involved
in weight reduction (Witmer, 1997), are the most purely
‘‘structural’’ in that they exclude primary roles in biomechanics or other physiological demands. Sherwood (1999)
regards these two functions as interrelated. Here, we
refer to bone mass reduction/maximum strength with
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
Fig. 11. Parasagittal sections at the level the maxillary
tooth row in Saguinus (a, b), Leontopithecus (c, d), Callithrix
(e, f), and Saimiri (g, h). Note that alveolar bone of the maxilla
is absent at the level of the third deciduous premolar (dp4) and
M1 in Saguinus and Callithrix. Osteogenesis of the alveolar
portion of the maxillary bone (arrows) at these levels is more
advanced in Leontopithecus and Saimiri. dc, deciduous canine;
dp2, first deciduous premolar; dp3, second deciduous premolar;
or, orbit. Scale bars, a, c, e, f, 1 mm; b, d, f, h, 150 lm. The
background in low-magnification images (a, c, e, g) was digitally altered, because the lighting was unbalanced; portions
of the image containing tissue were not altered. [Color figure
can be viewed in the online issue, which is available at
wileyonlinelibrary.com.]
minimal material as sinus functions postulated in the
‘‘structural hypothesis.’’
Pneumatization is viewed as an active growth process
by many investigators (Koppe et al., 1994, 1999; Witmer,
1995, 1997, 1999; Sherwood, 1999; Farke, 2008). Witmer
(1995, 1999) asserts that pneumatic mucosae opportunistically progress in the wake of an ‘‘osteclastic front’’
(1999, p 22), and observations of the earliest stages of
maxillary sinus pneumatization in primates support this
claim (Smith et al., 2005). According to some authors,
this reflects an obligatory growth process. For example,
Koppe and Nagai (1999) suggest that the pneumatic cavities have their ‘‘own developmental potential.’’ Conceptually, this recalls Moss and Greenberg’s (1967) concept
of a ‘‘pneumatic skeletal unit.’’ In this view, the sinus
mucosa is a functional matrix, a soft tissue structure
that exerts an epigenetic influence on the bones that it
borders (i.e., the skeletal unit).
403
In Witmer’s (1997) ‘‘epithelial’’ hypothesis, an idea
relating to the mechanism of pneumatization at the tissue
level, the sinus mucosa expands opportunistically. Paired
with the structural hypothesis, as articulated earlier, this
implies that the bone is resorbed by pneumatic mucosa
wherever possible. This, in turn, means that there are
limits to pneumatization, and these limits appear to
include sutural boundaries [see Sherwood (1999)], adjacent parts of teeth or tooth follicles (Smith et al., 2005), or
adjacent functional matrices (Schaeffer, 1920; Rossie,
2003; Smith et al., 2010). The cranial functional matrices,
dentition, and their supporting skeletal units may then be
viewed as specific regional elements that may either
‘‘permit’’ or constrain pneumatic expansion (Rossie, 2003;
Nishimura et al., 2005; Smith et al., 2005, 2010).
If grounded in functional matrix theory, the hypothesized ‘‘constraint’’ of sinus expansion by orbital, dental,
neural, or other tissues (Smith et al., 2005, 2010; Rossie,
2006) could include primacy of certain matrices. Rossie’s
(2006) view that the lack of pneumatization in some
New World monkeys (e.g., Saimiri and Cacajo) may be
related to extremes in approximation of the orbits or palatal proportions can be rooted in growth patterns of soft
tissues or dentition that border the paranasal spaces.
For instance, the maxillary dentition exerts localized
influence on paranasal spaces as individual dental follicles form osseous capsules (Marks and Schroeder,
1996); erupting teeth are considered osteogenic structures as well (Schroeder et al., 1992). Some of the alveolar bone formed around teeth or tooth follicles also form
part of the lateral and/or inferior wall of the maxillary
sinus, thus sharing portions of the hypothetical ‘‘pneumatic’’ skeletal unit. Here, we demonstrate that palatal
and nasal proportions and relative tooth size differ significantly among several species of New World monkeys.
Although sample sizes were likely too small to detect
all differences, post hoc tests did not support a hypothesis that relative tooth size was significantly larger in
Saimiri compared to all the callitrichines. Indeed, follicles of deciduous teeth are relatively larger or nearly
as large in Leontopithecus compared to Saimiri, especially relative to cranial length (although cranial length
may be a poor proxy for cranial size because of the
extreme dolichocephaly exhibited by Saimiri). However,
Figures 13 and 14 show a slight shift in the anteroposterior tooth follicle size gradient among species. All species
show a similar anteroposterior trend in relative size,
with large deciduous canines, gradually increasing deciduous premolar size and a smaller M1. The decreasing
gradient of relative size of the teeth, in particular, would
likely be associated with more ‘‘unneeded’’ bone in the
callitrichines compared to Saimiri. This is in keeping
with reports on older-aged specimens of each species.
The sinus eventually extends beyond M1 in Saguinus
(Smith et al., 2010), Leontopithecus (Rossie, 2006), and
overlaps M1 in Callithrix (Nishimura et al., 2005; Smith,
unpublished observations). Saimiri diverges from the
callitrichines at dp4 and especially M1 (see Fig. 14).
Results on HA density establish that the anteroposterior
pattern of mineralization is likewise different among the
species and suggest that the pace of mineralization in
the posterior maxillary teeth may be more rapid in Saimiri compared to callitrichines (see Fig. 15). A comparatively accelerated rate of development at dp4 and M1
could easily explain our previous observation that the
maxillary recess of Saimiri fails to expand beyond the
level of P4 postnatally (Smith et al., 2010). The relaAmerican Journal of Physical Anthropology
404
T.D. SMITH ET AL.
Fig. 12. Distribution of osteoclasts and osteoblasts (Ob) as seen in coronal sections of Saguinus (a, inset), Leontopithecus (b–d),
Callithrix (e), and Saimiri (f, g) at the level of the last deciduous premolar. In the callitrichines, the inferomedial surfaces of the
orbit were mostly depository on the orbital side (double arrows, rows of osteoblasts). In the contralateral (i.e., nasal), surfaces had
numerous osteoclasts (open arrows) and ‘‘scalloped’’ surfaces. In Saimiri, the inferomedial surface of the orbit was resorptive on the
orbital surface and depository on the nasal side (inset, f). In the floor of the orbit, the orbital surface of the maxilla was resorptive
as well (g) with deposition on the alveolar side (see inset). CR, remnants of the cartilaginous nasal capsule; Gl, glands; M, maxilla;
NC, nasal cavity; NS, nasal septum; Oc, osteocytes. Scale bars: (a) 1 mm (inset 20 lm); (b) 1 mm (inset 200 lm); (c) 200 lm; (d) 20
lm; (e) 1 mm (inset 200 lm); (f) 1 mm (inset 200 lm); (g) 1 mm (inset 200 lm). [Color figure can be viewed in the online issue,
which is available at wileyonlinelibrary.com.]
American Journal of Physical Anthropology
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
Fig. 12.
(Continued)
tively large size of the deciduous maxillary teeth in
Leontopithecus appears to weaken this argument, given
that the anteroposterior and superoinferior extent of the
maxillary sinus is most extreme in this species at birth
(Figs. 2 and 5).
Midfacial spatial characteristics, in concert with relative size of dp4 and M1, offers a better explanation for
the lack of pneumatization in Saimiri. Micro-CT recon-
405
structions suggest that the orbits are less convergent in
all callitrichines than Saimiri at this early stage (see
Fig. 8), in accord with the greater orbital convergence
reported in adult Saimiri compared to callitrichines
(Ross, 1995). Hartwig (1995) suggests that orbital
approximation is particularly extreme at birth in Saimiri. Thus, the relatively advanced neural development
of infant squirrel monkeys (Hartwig, 1995; Leigh, 2004)
may amplify orbital encroachment toward midline structures and spaces. The different extent of nasal fossa
compression between Saimiri and callitrichines is most
apparent from the levels of dp3 to M1 (see Figs. 6–8).
Bizygomatic–interorbital indices support the idea that
the orbit compresses the nasal fossa to a differing degree
among species at the level of M1 (see Fig. 17).
Collectively, midfacial indices reveal complexity
among the species. Palatonasal indices indicate that
position of the tooth follicles is closely adjacent to the
nasal fossa at all levels in Saimiri, whereas the palatonasal indices increase in all callitrichines from dp3
to M1 levels. Bizygomaticonasal indices show that the
proportions of the nasal cavity relative to overall facial width is most different between Saimiri and
Leontopithecus, and bizygomatic–interorbital ratios
reveal that orbital contents compress the nasal region
to a greater extent in Saimiri than Leontopithecus at
M1. Although Callithrix has a relatively compressed
nasal fossa at M1, it has the lowest palatonasal index
at this level.
Taken together, our findings suggest that large relative tooth size alone is not sufficient to prevent pneumatization. The different developmental outcomes in Leontopithecus and Saimiri are best explained by differences
in proximity of the orbit and tooth to the nasal region
(which, in turn, is dictated, in part, by size of the orbit
and teeth). Orbital cross-sectional area or volumes are
factors that we were unable to assess, because the orbits
were partially damaged in many of the specimens. Qualitatively, the orbits of Leontopithecus appear relatively to
be the smallest of the four species, while largest in Saimiri. Other architectural differences between the two
taxa, such as the greater vertical separation of the orbits
and palate in Leontopithecus (see Figs. 6 and 7), may
offer an additional explanation. More robust sample
sizes or alternative methods, such as three-dimensional
morphometric comparisons, are needed to confirm these
suggestions.
The constraining effect of structures such as the dentition and alveolar bone on the maxillary sinus has
been discussed many times regarding humans
(Schaeffer, 1920). Clinical data on humans support the
idea that this is largely due simply to adjacency, as
suggested by Koppe and Nagai (1999). For example,
pneumatic expansion of the maxillary sinus ensues following extraction of maxillary dentition [see (Sarnat,
1997), and references therein]. Moreover, distraction of
alveolar bone can be associated with enlargement of the
nasal airways (Cappellette et al., 2008), which may
indirectly affect paranasal spaces as well. Differences
among the New World monkeys in the perinatal period
show how extremes in patterns of pneumatic expansion
can be explained by positional factors. The osseous components of any given skeletal unit may relate to more
than one functional matrix (Moss and Greenberg,
1967), and therefore myriad skeletal growth outcomes
may be related to the interplay of growth patterns
among different functional matrices.
American Journal of Physical Anthropology
American Journal of Physical Anthropology
0.162/0.006*
0.133/0.005*
0.142/0.007*y
0.144/0.007
0.087/0.007
0.047/0.002*
0.038/0.001*
0.04/0.001*
0.042/0.002*
0.024/0.001
1168.04/45.07
1149.99/30.0
1138.44/62.85
968.93/20.96
1.4/0.09
1.33/0.06*
1.43/0.122
1.53/0.15
3.41/0.1*
3.65/0.19*
15.69/7.41
44.74/33.50*
1173.33/96.43
1085.75/63.06
1002.48/68.6
916.86/21.36
1.43/0.11
1.63/0.06*
1.57/0.06
1.54/0.07
3.88/0.15
3.83/0.21
82.22/65.59
73.52/48.72
M/SD
0.144/ 0.008
0.117/0.01
0.121/0.007*
0.126/0.015
0.076/0.015*
0.04/0.004
0.032/0.003
0.033/0.001
0.035/0.004
0.021/0.004
M/SD
Leontopithecus
rosalia (lion
tamarin)
59.11/58.85
83.54/50.72
3.93/0.21
4.43/0.25
1.38/0.11
1.52/0.16
1.64/0.15
1.76/0.1*
935.98/96.43*
822.84/116.96*
839.07/108.66*
792.95/120.5*
0.13/0.012*
0.108/0.01*
0.111/0.01y
0.126/0.01
0.08/0.013
0.036/0.038
0.03/0.003
0.03/0.004
0.034/0.003
0.021/0.003
M/SD
90.56/71.51
216.09/108.58*
4.52/0.29*
4.33/0.18*
1.30/0.06
1.39/0.12
1.35/0.2
1.35/0.08*
1267.94/98.12*
1208.75/124.3*
1181.79/74.84*
1163.23/143.17*
0.152/0.008
0.124/0.005
0.13/0.006
0.145/0.008
0.122/0.01*
0.034/0.002*
0.027/0.002*
0.029/0.002*
0.032/0.003*
0.025/0.004
M/SD
Species (common name)
Saimiri
boliviensis
(squirrel
monkey)
M, mean; SD, standard deviation; *,y, pairs of means that are significantly (P \ 0.05) different according to post hoc testing.
Tooth ratios
dc-PL
dp2-PL
dp3-PL
dp4-PL
M1-PL
dc-CL
dp2-CL
dp3-CL
dp4-CL
M1-CL
HA density
dc
dp2
dp3
dp4
Palatonasal indices
Dp2 PN index
DP3 PN index
Dp4 PN index
M1 PN index
Bizygomaticonasal indices
Dp4 ON index
M1 ON index
Bizygomatic–interorbital indices
Dp4 ON index
M1 ON index
Variable
Saguinus oedipus
(cotton-top
tamarin)
Callithrix
jacchus
(common
marmoset)
TABLE 3. Mean (6standard deviation) dental and midfacial variables in four species of monkeys with results of statistical analysis
X2 5 8.31, P \ 0.05
X2 5 8.44, P \ 0.05
X2 5 11.44, P \ 0.05
X2 5 11.95, P \ 0.01
X2 5 5.06, NS
X2 5 10.28, P \ 0.02
X2 5 7.98, P \ 0.05
X2 5 12.74, P \ 0.01
X2 5 9.86, P \ 0.05
X2 5 10.26, P \ 0.02
X2 5 11.66, P \ 0.01
X2 5 11.33, P \ 0.02
X2 5 10.27, P \ 0.02
X2 5 10.35, P \ 0.02
X2 5 12.83, P \ 0.01
X2 5 8.82, P \ 0.05
X2 5 10.83, P \ 0.02
X2 5 10.42, P \ 0.02
X2 5 9.37, P \ 0.05
X2 5 9.86, P \ 0.05
X2 5 8.28, P \ 0.05
X2 5 5.95, NS
Kruskal–
Wallis test
406
T.D. SMITH ET AL.
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
407
Fig. 14. Means for ratios of the cube-root of dental follicle
volume to palatal length (top) and cranial length (bottom),
showing the divergence of Saimiri from the callitrichines in relative size of posterior dentition. Error bars, standard error of
mean.
Fig. 15. Mean hydroxyapatite density of deciduous dentition
in the four species.
Fig. 13. Species comparison of means for ratios of the cuberoot of dental follicle volume to palatal length (left column) and
cranial length (right column). Error bars, standard error of
mean.
Bone-cell distribution and remodeling fields
Other growth principles may explain the extent of
pneumatization of the maxilla, at least in part. In vertical dimensions, for example, the maxillary sinus of
humans and some New World primates may be attributed to downward midfacial and anterior orbital growth
trajectories (Mauser et al., 1975; Enlow and Hans, 1996;
Smith et al., 2005). In humans, the ‘‘floor’’ of the maxillary sinus ‘‘drops’’ inferiorly, in tandem with resorption
that occurs during downward displacement of the maxilla. The ‘‘roof’’ of the maxillary sinus, and shared boundary with the orbit, shifts superiorly, in tandem with deposition on the orbit surface that accompanies forward
remodeling of the orbital cones during growth (the ‘‘V’’
principle—Enlow and Hans, 1996). Observations of bonecell distribution along the roof and floor of the maxillary
sinus in several species of callitrichines suggest that the
same growth processes may explain vertical expansion of
the sinus space (Smith et al., 2005). Here, we confirm
earlier observations on callitrichines, but, in Saimiri, orbital remodeling is markedly different.
Major differences in the distribution of bone cells
along the inferior and medial orbit, in the alveolar
region, and in some adjacent regions, are shown in Figure 18. A schematic view of a coronal section through
the level of dp4 is shown, with an illustration of distribution patterns detailed in Table 2. This dental follicle
level was selected for representation, because this dental
level is ultimately the posterior limit for the maxillary
recess in Saimiri (Smith et al., 2010). Distribution of
osteoclasts (2) and osteoblasts (1) is indicated to denote
resorptive and depositional surfaces, respectively. The
American Journal of Physical Anthropology
408
T.D. SMITH ET AL.
Fig. 16.
Palatonasal indices in the four species from the level of the first deciduous premolar (dp2) to M1.
Fig. 17. Bizygomaticonasal (left) and bizygomatic–interorbital (right) indices in the four species from the level of the last deciduous premolar (dp4) to M1.
American Journal of Physical Anthropology
MIDFACIAL MICROANATOMY OF PERINATAL MONKEYS
Fig. 18. Schematic diagrams showing patterns of osteoblast
(1) and osteoclast (2) distribution at the level of the last deciduous premolar in the four species. Note contrast in the inferomedial orbit between callitrichines (a–c) and Saimiri (d).
orbital surface of the maxilla was mostly depositional in
callitrichines (Fig. 18a–c), but was mostly resorptive in
Saimiri (Fig. 18d). At the level of dp4, the medial wall of
the orbit is a depositional surface in perinatal Leontopithecus and Callithrix and is resorptive in Saguinus and
Saimiri. However, the inferomedial margin of the orbit
is depositional at this level in all callitrichines, in contrast to the nearly uniform resorption typical of medial,
inferomedial, and inferior surfaces of the maxilla in Saimiri (Fig. 18d).
The pattern of a superior shift in the floor of the orbit
in callitrichines closely resembles the prenatal human
pattern (Mauser et al., 1975) and, as in humans, is
clearly related to vertical expansion of the maxillary
sinus. Such a pattern might be regarded as a ‘‘passive’’
mode of sinus enlargement, a descriptor offered by Weidenriech (1924) regarding the very nature of sinuses.
Noteworthy in this regard is Enlow and Hans’ (1996)
concept of paranasal sinuses as ‘‘leftover ‘dead’ unused’’
(p 143) spaces created as a byproduct of enlargement by
neighboring craniofacial bones. In that view, particular
boundaries of the maxillary sinus expand outward by following remodeling ‘‘growth fields’’ of the maxillary bone.
Enlow and Hans (1996) did not discount epigenetic
effects of soft tissues as important factors in craniofacial
growth. The different remodeling patterns seen in Saimiri are most certainly related to our qualitative observations of the degree of perinatal orbital approximation
and high-bizygomatic–interorbital indices. The limitations imposed by orbital encroachment thus provide an
extreme example of why pneumatization patterns differ
so profoundly among New World monkeys (Rossie, 2006).
CONCLUSIONS
Previously, we suggested orbitonasal proportions and
relative size of the dentition factor prominently in pre-
409
venting pneumatic expansion of the maxillary recess in
Saimiri (Smith et al., 2010). Here, differences in relative
size of dp4 and M1 among species provide a strong explanation for the observation that the maxillary recess
in Saimiri fails to expand beyond the level of P4 (Smith
et al., 2010). As previously suggested, relative size of the
dentition appears not to be the sole explanation. Saimiri
is exceptionally different from callitrichines in degree of
orbital approximation and in the pattern of orbital
remodeling at birth. Overall, it is notable that tooth-palate size ratios show different patterns than tooth-cranial
size ratios: compared to the callitrichines, maxillary
teeth in Saimiri are large relative to palate but not cranial length (see Fig. 13). These different patterns indicate that the deciduous teeth are large relative to the
midface, but not relative to overall head size in perinatal
Saimiri. Thus, orbital contents [see Hartwig (1995)] and
dentition are more tightly ‘‘packed’’ in the midface of
perinatal Saimiri relative to the callitrichines. Although
a constraining influence of the main nasal chamber on
the maxillary recess cannot be discounted, preliminary
findings indicate that the surface area of the recess
increases isometrically relative to the main nasal chamber, in apparent contrast to disproportionately higher
rate of sinus expansion (relative to the nasal fossa) in
Saguinus (Smith et al., 2010).
Comparisons among other species would bolster the
hypothesis that the packing of dental and orbital matrices is the most important factors in constraint of pneumatization, and a comparison of perinatal cercopithecoids (many of which lack true maxillary sinuses) would
be most informative. The divergence of M1 from the pattern seen for the other teeth is interesting in light of the
different patterns of brain growth seen in Saimiri compared to Saguinus fuscicollis (Leigh, 2004). Brain growth
is more rapid in Saimiri, being complete by six months
of age, while brain growth is more prolonged in the tamarin. If these neural differences reflect a contrast
between Saimiri and callitrichines, in general, it suggests that life history may have an indirect influence on
constraint of pneumatic expansion via the high correlation of M1 development and brain growth. Similarly,
Rossie (2006) hypothesized that the selection for precocial neonates may be linked to the loss of the maxillary
sinus in Saimiri, which likewise suggests the need for
investigation of perinatal cercopithecoids.
ACKNOWLEDGMENT
We thank L.T. Nash for suggestions regarding post hoc
statistical tests.
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