BRIEF REPORT Clinal Variation of Maxillary Sinus Volume in Japanese Macaques (Macaca fuscata)
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Macaques (genus Macaca) are unique among cercopithecids in that they possess a maxillary sinus, and among anthropoids in that they demonstrate a relatively weak relationship between the size of this sinus and the cranium. To test the hypothesis that extrinsic factors may contribute to maxillary sinus size variation, a sample of 46 Japanese macaque (M. fuscata) crania from known localities were subjected to computed tomography (CT) imaging, and sinus volume and nasal cavity area were analyzed relative to latitude and temperature variables. The results suggest that the environmental factors are significant determinants of nasal cavity size in Japanese macaques, but that the relationships between the environment and maxillary sinus volume (MSV) are probably a passive consequence of changes in the size of the nasal cavity. The sinus shrinks as the nasal cavity expands, due to an increased need to condition inspired air in colder climates. This in turn suggests that the sinus itself does not contribute significantly to upper respiratory function. Am. J. Primatol. 59:153–158, 2003. r 2003 Wiley-Liss, Inc.Keywords:
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Sinus (botany)
Bergmann's rule
Variation (astronomy)
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The function and evolution of paranasal pneumaticity remains elusive, in part because of limited sampling and description. Here, the frontal sinuses from 62 species of bovids were investigated using X-ray computed tomography. This survey revealed hitherto undescribed diversity in the morphology of this sinus, and suggests that it was probably present in the common ancestor of Bovidae. Among extant bovids, the frontal sinuses were lost or reduced to recesses at least six different times. Quantitative analyses, when accounting for phylogeny using phylogenetically independent contrasts, did not find any link between the size or complexity of the frontal sinus and head-to-head ramming behaviour. Other analyses indicated that frontal sinus size was correlated most closely with the size of the frontal bone itself, rather than with the overall skull size or horn size. These results may be partially consistent with the hypothesis of sinuses being the result of 'opportunistic pneumatization', in which sinus size depends on the quantity of bone available for pneumatization as well as the mechanical demands placed on the skull. Additional evidence also indicates a strong phylogenetic correlation with sinus morphology, particularly with regard to the presence of paranasal diverticula, as well as the ability of sinuses to cross sutural boundaries.
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Differential Scaling Patterns in Maxillary Sinus Volume and Nasal Cavity Breadth Among Modern Humans
Among modern humans, nasal cavity size and shape reflect its vital role in air conditioning processes. The ability for the nasal cavity to augment its shape, particularly in inferior breadth, likely relates to the surrounding maxillary sinuses acting as zones of accommodation. However, much is still unknown regarding how nasal and sinus morphology relate to each other and to overall craniofacial form, particularly across diverse populations with varying respiratory demands. As such, this study uses computed tomographic (CT) scans of modern human crania (N = 171) from nine different localities to investigate ecogeographic differences in (1) the interaction between maxillary sinus volume (MSV) and nasal cavity breadth (NCB) and (2) scaling patterns of MSV and NCB in relation to craniofacial size. Reduced major axis (RMA) regression reveals that all samples exhibit an inverse relationship between MSV and NCB, but statistical significance and the strength of that relationship is sample dependent. Individuals from cold-dry climates have larger MSVs with narrower NCBs, while smaller MSVs are associated with wider NCBs in hot-humid climates. MSV and NCB each scale with positive allometry relative to overall craniofacial size. However, sample differences are evident in the both the interaction between MSV and NCB, as well as their correlation with craniofacial size. While these results provide further support that the maxillary sinus and nasal cavity are integrated among populations from opposite ends of the climatic spectrum, additional epigenetic factors are needed to explain variation of these structures among populations from more intermediate climates.
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Atlas bridging represents the formation of a bony bridge over the vertebral artery groove of the first cervical vertebra. There are two kinds of bridging, the ‘posterior bridge’ and the ‘lateral bridge’. Such bridges may occur together or separately, and bilaterally or unilaterally. We investigated ontogenetic change and geographical variation of atlas bridging in Japanese macaques (Macaca fuscata) to clarify age effects and frequencies within a species. A total of 193 skeletal specimens of Japanese macaques of known chronological age were examined for ontogenetic change. Atlas bridges, both posterior and lateral, were present in most adults; they were found to develop at an early age. The posterior and lateral bridges were found complete at around 400–830 and 700–2500 days, respectively, after birth. A total of 328 Japanese macaques (Macaca fuscata fuscata and Macaca fuscata yakui) from seven regions were used in the study of geographical variation. Both posterior and lateral bridges were commonly observed regardless of region, with a tendency for a slightly lower prevalence of the lateral bridge than the posterior bridge. Atlas bridging did not differ in frequency between the right and left sides. Sexual differences were not significant in most of the populations. As for the lateral bridge, the Shimane population had a lower frequency than that found in the other populations. However, even considering such intraspecific variation, atlas bridging can be considered as a stable trait within Japanese macaques, the prevalence of which is remarkably higher than in hominoids.
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Extant African apes and humans share the frontal sinus while extant Asian apes don't. The analysis of the frontal sinus is essential for understanding the evolution of the great apes as well as the role of the paranasal sinuses. However, there is no concrete agreement on the phylogenetic and functional interpretations of the frontal sinus. Partly, this is due to the paucity of morphological information of the frontal sinus in African apes including ontogenetic and individual variations. This study examined the three-dimensional morphology of the frontal sinus in twelve chimpanzees' crania by using the Computed Tomography.The frontal sinus in the chimpanzee grows upward from the nasal cavity and reaches the level of the superior orbital margin at the same chronological age as in humans. This fact probably suggests that the growth of the sinus in the chimpanzee is different from that in humans in terms of the biological age determined by dental development.The frontal sinus morphology in the chimpanzee is as variable as that in Homo sapiens. The sinus volume clearly correlates with the cranial maximum length and scales in a positive allometric fashion relative to the length. The protrusion of the frontal sinus in the interorbital region is also related with the length.The interspecific difference in the morphology of the frontal sinus between adult chimpanzees and humans is possibly resulted from the morphological difference of the skull and body size.
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Sinus (botany)
Troglodytes
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Homo sapiens
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Abstract Previous studies exploring the effects of climate on the nasal region have largely focused on external craniofacial linear parameters, using dry crania of modern human populations. This investigation augments traditional craniofacial morphometrics with internal linear and volumetric measures of the anatomic units comprising the nasal complex (i.e., internal nasal cavity depth, maxillary sinus volumes). The study focuses on macaques (i.e., Macaca mulatta and Macaca fascicularis ) living at high and low altitudes, rather than on humans, since the short residency of migratory human populations may preclude using them as reliable models to test the long‐term relationship of climate to nasal morphology. It is hypothesized that there will be significant differences in nasal complex morphology among macaques inhabiting different climates. This study integrated three different approaches: CT imaging, comparative anatomy, and morphometrics—in an effort to better understand the morphological structure and adaptive nature of the nasal complex. Results showed statistically significant differences when subsets of splanchnocranial and neurocranial variables were regressed against total maxillary sinus volume for particular taxa. For example, basion–hormion was significant for M. fascicularis , whereas choanal dimensions were significant only for M. mulatta . Both taxa revealed strong correlation between sinus volume and prosthion to staphylion distance, which essentially represents the length of the nasal cavity floor—and is by extension an indicator of the air conditioning capacity of the nasal region. These results clearly show that climatic effects play a major role in shaping the anatomy of the nasal complex in closely related species. The major influence upon these differing structures appears to be related to respiratory‐related adaptations subserving differing climatic factors. In addition, the interdependence of the paranasal sinuses with other parts of the complex strongly indicates a functional role for them in nasal complex/upper respiratory functions. Anat Rec, 291:1420–1445, 2008. © 2008 Wiley‐Liss, Inc.
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This study explores variation, covariation, and ecogeographic pattern of the nasal cavity, maxillary sinuses, and external midfacial skeleton across 15 populations of east Asian origin inhabiting the Far East, Siberia, Alaska and Greenland.We have collected linear measurements of the internal nasal cavity, maxillary sinus and external midfacial skeleton as well as volumes and surface areas of three-dimensional models of the cavity. A set of seven climatic variables, mtDNA and Y-chromosome genetic matrices and a matrix of geographic distances were also utilized.A strong association between form of the nasal cavity and climate was found, whereby all north Asian groups display increased volumes, areas and lengths of the cavity, and surface area to volume ratios (SA/V). Most of Siberian groups exhibit not only large and long, but also wide and tall nasal cavity. The Eskimo-Aleutian speaking groups possess cavities that are vertically short and narrow but of a high SA/V ratio. The sinuses exhibit an exceptionally high level of within- and between-group variation which supports the views on the sinus as an architectural byproduct. Both volume and area of the nasal cavity can be reliably estimated based on a set of simple and repeatable linear measurements.While the nasal cavity and maxillary sinus are both larger in a larger facial skeleton, there is a strong inverse relationship between them at a given facial size. Our results do not support the notion that the shape of the internal nasal cavity is more strongly associated with climate compared to the external midfacial morphology.
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Mammal skulls contain up to four mucosal-lined, air-filled cavities called paranasal sinuses within the bones surrounding the nasal chamber, including the maxilla, ethmoid, sphenoid, and frontal. Paranasal sinuses are highly variable in presence and morphology among mammals, and their function is not well understood due to the fact that they are hidden within the skull and inaccessible without use of destructive methods. The leading hypothesis to explain sinus function is that they opportunistically form where bone is mechanically unnecessary. Sinuses may also help dissipate stress more evenly across the skull during feeding and other behaviors. To test these hypotheses, I conducted the first quantitative and comparative investigation of how frontal sinus morphological disparity relates to skull morphology, ecology and diet in mammalian carnivores. To do so, I used non-destructive CT scans and applied a novel technique to quantify the three-dimensional shape of sinuses. Cranial shape, body size, diet, and ecology vary markedly within Carnivora, with many examples of convergence, making them an ideal framework within which to examine sinus function. I quantified frontal sinus morphology for fifty-six carnivore species, including a large intraspecific sample of coyotes (Canis latrans) with associated age and diet information. Results support the hypothesis that frontal sinuses from where bone is mechanically unnecessary, but several taxa lacked frontal sinuses, suggesting that there may be phylogenetic constraints on which taxa can develop frontal sinuses. Among Carnivora with frontal sinuses, sinus morphology was strongly correlated with the size and shape of the frontal bone, and was also correlated with allometric differences in skull shape between families that relate to biomechanical function. Skull shape disparity related to ecology also appears to affect frontal sinus morphology. Dorsal flattening of the skull roof in aquatic and fossorial carnivores was associated with reduced or absent frontal sinuses. Large, anteriorly oriented eyes and foreshortened snouts of arboreal species also appear to limit space where a sinus can form. Intraspecific variation in sinus shape suggests frontal sinus morphology is affected by diet-related skull utility, and that frontal sinus morphology can vary throughout an organism's life and be modified to improve skull performance.
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Carnivore
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Frontal bone
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In contrast to the paranasal sinuses of Old World monkeys and hominoids, little information is available about the paranasal sinuses of New World monkeys. Because this information is crucial in order to draw further conclusions about the evolution and biological role of skull pneumatization, this study investigates the morphology of the paranasal sinuses in adult black-and-gold howler monkeys (Alouatta caraya). Volumes of the paranasal sinuses were calculated using computer software (SURFdriver or Allegro) from serial coronal CT scans of 20 skulls of both sexes. Skull pneumatization in A. caraya is more complex than in other higher primates. In both sexes, the maxillary sinus (MS) is the only pneumatic cavity and enlarges regularly into neighboring bones such as the frontal bone and the basisphenoid. The resulting pansinus is often partitioned by several vertical septa. As in most external cranial dimensions, mean MS volume of A. caraya (male 4.08 cm(3); female 2.00 cm(3)) shows significant sexual dimorphism. Reduced major axis regression analysis between MS volume and different cranial dimensions for A. caraya (and for available data from other platyrrhines) suggests a distinct association for this group, with Alouatta having one of the largest pneumatic cavities. The combination of this unusual expansion of the MS of Alouatta and the occurrence of distinct septa within the sinus may be a consequence of the distinct skull architecture of Alouatta.
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Abstract In order to investigate craniofacial size and three-dimensional shape variations independently in the Japanese macaque ( Macaca fuscata ) we used a geometric morphometries technique. A total of 55 specimens were CT scanned to generate a three-dimensional model of each cranium, and 57 landmarks were digitized to analyze the craniofacial shape variation in the Japanese macaque. The results showed that four intra-specific groups, consisting of two subspecies and the two sexes, differed in both size and shape space. In size, the cranium of the Macaca fuscata yakui (MFY) was smaller than that of Macaca fuscata fuscata (MFF) in both sexes, and female crania were smaller than male crania in both subspecies. Shape sexual dimorphisms in both subspecies were detected in the first axis of principal component analysis and were related to a relatively broad orbit, smaller neurocranium, enlarged snout, and broader temporal fossa in males. The shape differences between subspecies showed different features than those between sexes. Male subspecies shape differences were detected in the first and third axes, while those for females were in the first and second axes. Subspecies shape differences common to both sexes were a narrower orbit, relatively small neurocranium, longer snout, and postorbital constriction in MFY. Male MFY was specifically characterized by a more anterior and superior direction of snout protrusion. In contrast, female MFY showed an inferior direction of snout protrusion. Female MFY also had a taller orbit. With regard to the relationship between size and shape differences, shape sexual dimorphism for each subspecies was positively associated with size difference, but there was no such association between subspecies in either sex. Size does not seem to play an important role in subspeciation of Macaca fuscata.
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There is considerable speculation about the role and significance of the para-nasal sinuses in the Hominoidea, and this study aims to present new data about an old problem from cephalograms of dried crania. Measurements of frontal sinus volumes were determined for Gorilla gorilla gorilla; G. gorilla beringei and Pan troglodytes. By adopting an allometric approach it was determined that (1) the frontal sinus volume of Gorilla is relatively smaller than that of Pan, and that the frontal sinus of G. g. gorilla is relatively smaller than that of G. g. beringei. (2) Frontal sinus volume scales in a positive allometric fashion relative to skull length. Since the slope is steeper for Pan, frontal sinus volume is increasing at a faster rate than in Gorilla. Sexual dimorphism in frontal sinus volume is present. Thirty crania of Pongo were investigated for evidence of pneumatization of the frontal bone. In no case was secondary invasion of the frontal bone by the maxillary antrum observed. (3) In Gorilla, the nasal cavity volume scales isometrically with skull length. The scaling relationships discussed do not support any ‘functional’ role of the frontal sinus associated with nasal function but suggest a ‘structural’ role associated with craniofacial architecture.
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Frontal sinus
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Sinus (botany)
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