Dietary correlates of temporomandibular joint morphology in New World primates
Introduction
Temporomandibular joint (TMJ) form has been documented to vary both within humans (Sullivan, 1917, Weidenreich, 1943, Hinton and Carlson, 1979, Harvati, 2001, Lockwood et al., 2002, Terhune et al., 2007) and across primates as a whole (Weidenreich, 1943, Ashton and Zuckerman, 1954, Bouvier, 1986a, Bouvier, 1986b, Wall, 1995, Vinyard, 1999, Lockwood et al., 2002). The more recent of these analyses have directly linked aspects of this variation to functional differences among taxa in the masticatory apparatus (e.g., Bouvier, 1986a, Bouvier, 1986b, Wall, 1995, Wall, 1999, Vinyard, 1999, Vinyard et al., 2003). Building upon experimental analyses of masticatory function by Hylander and colleagues (e.g., Hylander, 1975, Hylander, 1979, Hylander and Bays, 1978, Hylander and Bays, 1979, Hylander and Crompton, 1980), Smith et al. (1983) and Bouvier, 1986a, Bouvier, 1986b first analyzed the biomechanical scaling of the TMJ both across anthropoids (Smith et al., 1983) and separately within cercopithecoids (Bouvier, 1986a) and platyrrhines (Bouvier, 1986b). More recent work by Wall and Vinyard (Wall, 1995, Wall, 1999, Vinyard, 1999, Vinyard et al., 2003) has more explicitly tested functional hypotheses related to TMJ shape in both anthropoids and strepsirrhines. All of these studies suggest that the form of the TMJ covaries with differences in feeding behavior among primates, principally in the dimensions of the joint (and particularly the mandibular condyle) in relation to load resistance, use of the anterior or posterior dentition, and relative gape.
Following on this research, it is the goal of this study to examine variation in TMJ morphology in the context of functional and dietary differences among New World primates. Platyrrhines are an excellent group to test this proposed association between feeding behavior and TMJ morphology for a number of reasons. Taxa within this clade vary considerably in their feeding behavior and body size, ranging from an annual fruit intake of as little as 8% in Cebuella to as much as 86% in Ateles (Norconk et al., 2009), and with body sizes varying between 0.11 and 11.4 kg in Cebuella pygmaea and Alouatta pigra, respectively (Smith and Jungers, 1997). Importantly, masticatory variation in this group has been extensively evaluated (e.g., Kinzey, 1974, Hylander, 1975, Kay, 1975, Rosenberger and Kinzey, 1976, van Roosmalen et al., 1988, Ayres, 1989, Rosenberger and Strier, 1989, Kinzey, 1992, Kinzey and Norconk, 1993, Anapol and Lee, 1994, Spencer, 1995, Wright, 2005, Constantino, 2007, Taylor and Vinyard, 2009, Norconk et al., 2009), and the material properties of food items ingested by a number of species in this clade have been comparatively well documented (Kinzey and Norconk, 1990, Wright, 2005, Norconk et al., 2009, Wright and Wright, 2010, Chalk et al., 2010). This study analyzed TMJ variation in this clade in two ways. First, TMJ morphology across the entire sample was quantified using geometric morphometric methods, and the extent to which this variation covaries with feeding behavior and body size was examined. Second, three separate sets of phylogenetically restricted pairwise comparisons were performed. These comparisons were designed to test a series of morphological predictions for TMJ shape based on existing experimental and behavioral data. These morphological predictions and their biomechanical basis are outlined in the following section and the ecological data for each of the comparative groups is reviewed.
Theoretical and experimental analyses of masticatory function have demonstrated that the magnitude of the joint reaction force varies depending upon the position of the bite point, the magnitude and position of the muscle resultant force, position of the TMJ in relation to the tooth row, as well as the overall geometry of the masticatory apparatus (e.g., Hylander, 1975, Hylander, 1979, Hylander, 2006, Greaves, 1978, Smith, 1978, Hylander and Bays, 1979, Brehnan et al., 1981, Spencer, 1995, Spencer, 1999). For example, more anterior bite points produce relatively higher joint reaction forces (JRF), and the ratio of the JRF between the working and balancing sides becomes smaller as the bite force moves more posteriorly. Histological, experimental, and comparative studies have also shown that the loading within the joint is unlikely to be uniform (e.g., Moffett et al., 1964, Hylander, 1979, Hylander, 2006, Richards, 1987, Richards, 1988).
Bony morphology may also help to facilitate or limit movements at the joint. These movements primarily occur in the anteroposterior and mediolateral planes and include rotation and translation of the condyle, or a combination of these two movements. During simple opening and closing movements of the mandible (as would occur with social display behaviors or incision, as well as at the beginning or end of a gape cycle during mastication), motion of the right and left condyles should be roughly equal, and is typically comprised of a combination of translation and rotation in primates (i.e., sagittal sliding). Cineradiographic analyses conducted by Wall, 1995, Wall, 1999 indicate that sagittal sliding of the condyle is strongly correlated with linear gape between the incisors. By contrast, mastication occurs along the postcanine dentition and is characterized by mediolateral deviation of the mandible. This type of movement typically involves only slight rotation and lateral movement of the working side condyle with the balancing side condyle shifting downward (or forward) and medially along the (variably prominent) articular eminence (Byrd et al., 1978, Miyawaki et al., 2000, Komiyama et al., 2003, Hylander, 2006). Analyses of masticatory movements during the comminution of foods with different food material properties suggest that with more resistant foods, the amount of lateral deviation increases (Byrd et al., 1978, Anderson et al., 2002, Komiyama et al., 2003, Wall et al., 2006; but see Reed and Ross, 2010).
Although there are many factors that are likely to affect both force and range of motion at the TMJ, this study focuses on three (non-mutually exclusive) influences: food material properties, location of the bite point, and gape requirements. First, the material property of a food item influences the amount of muscle force required to process the food, which, in turn, influences the magnitude of the joint reaction force at the TMJ (e.g., Lucas, 2004, Williams et al., 2005). Second, the location of the bite point will influence the amount of muscle and bite force vs. joint reaction force, as well as the distribution of the joint reaction force across the balancing and working side condyles (e.g., Hylander, 1979, Hylander and Bays, 1979, Brehnan et al., 1981). Finally, behavioral and dietary demands associated with gape requirements (e.g., social display behaviors such as canine displays and/or food object size) are particularly likely to influence range of motion at the TMJ (e.g., Lucas, 1981, Lucas, 1982, Wall, 1995, Wall, 1999, Vinyard et al., 2003, Hylander and Vinyard, 2006, Hylander et al., 2008). Based on this previous research regarding TMJ biomechanics, I generate a series of predictions regarding how TMJ forms are expected to vary in association with these factors in three separate clades of platyrrhines:
- 1)
The surface area of the mandibular condyle should be relatively larger in taxa that masticate more resistant food objects and/or use their anterior dentition extensively for food processing. Increased joint reaction forces at the TMJ (as a consequence of increased muscle resultant forces and/or use of the anterior dentition) should necessitate relatively larger joint surface areas in order to improve the load resistance capabilities of the TMJ by increasing the area over which force is applied (Hylander, 1979, Smith et al., 1983, Bouvier, 1986a, Bouvier, 1986b, Taylor, 2005).
- 2)
The anteroposterior length of the TMJ will vary in association with the frequency of ingestive behavior. Taxa that use their anterior teeth extensively for ingestive behaviors (particularly large object feeders that must also generate large jaw gapes) should have a relatively anteroposteriorly elongated cranial articular surface (e.g., the glenoid should be anteroposteriorly longer in relation to condylar length so that more sagittal sliding can occur at the joint) (Wall, 1995, Wall, 1999, Vinyard et al., 2003).
- 3)
The mediolateral width of the TMJ will vary as a consequence of the frequency of masticatory behaviors. Studies of joint remodeling and dysfunction have suggested that the lateral aspect of the TMJ experiences higher stresses than other portions of the joint (Moffett et al., 1964, Richards and Brown, 1981, Hinton, 1981, Richards, 1988). These increased stresses may be a result of twisting of the mandibular corpus and compression of the lateral aspect of the condyle during the power stroke and/or lateral shifting of the working side condyle during lateral deviation of the mandible (Hylander, 1979, Hylander and Bays, 1979, Bouvier, 1986a, Bouvier, 1986b; Taylor, 2005, Taylor, 2006). Consequently, it is predicted here that taxa masticating hard- and/or tough-food objects will exhibit mediolaterally expanded joint surfaces to withstand the increased stresses generated by increased twisting and lateral deviation of the mandible during mastication. This will be particularly true of taxa where the frequency (rather than just the magnitude) of the power stroke is increased (i.e., tough object feeders) and/or where intensive unilateral mastication of food items is emphasized (as with taxa that masticate hard- and/or tough-food objects on the postcanine dentition). 4) The entoglenoid process will be relatively larger in resistant-object feeders and taxa that use their postcanine dentition extensively for unilateral mastication when compared with taxa that do not rely heavily on unilateral mastication on the posterior teeth. Work by Wall, 1995, Wall, 1999 demonstrated that the mandibular condyle contacts the entoglenoid process during masticatory movement, and that size and shape of the entoglenoid process and mandibular condyle were correlated. Functionally, Wall (1999) interpreted this congruence to indicate that the entoglenoid process acts to guide the mandibular condyle during sagittal sliding, and possibly to prevent excessive mediolateral movements. Thus, a relatively large entoglenoid process may serve to guide medial movements of the balancing side condyle during mastication and to increase joint surface area and reduce joint stresses. 5) The articular tubercle should be relatively larger in resistant-object feeders compared with soft-object feeders. As the primary attachment site of the temporomandibular ligament (TML), the size of the articular tubercle is likely a reflection of the size of the TML (Wall, 1995). This ligament has been suggested to function to maintain contact between the mandibular and cranial components of the TMJ, therefore resisting tensile forces at the joint (Greaves, 1978, Hylander, 1979, Spencer, 1995, Wall, 1995). Sun et al.’s (2002) analysis of the TMJ tissues of miniature pigs concluded that the primary function of the lateral joint capsule was to stabilize the TMJ when the condyle performs lateral movements, such as during lateral deviation. It is therefore predicted that relatively larger articular tubercles should be found in taxa that exhibit increased lateral deviation (e.g., resistant-object feeders and taxa that use their postcanine dentition extensively for unilateral mastication) (Byrd et al., 1978, Anderson et al., 2002, Komiyama et al., 2003, Wall et al., 2006, but see Reed and Ross, 2010).
Analyses of TMJ shape were performed by examining three sets of closely related taxa with different feeding behaviors and diets: atelines, cebines, and pitheciines. This approach allows for multiple pairwise comparisons of TMJ morphology among closely related taxa in a single clade, thereby minimizing the effects of phylogeny on shape differences. The following section outlines the dietary ecology of the members of each of the comparative groups, reviews previous morphological findings for these species, and lays out the expected variation in TMJ morphology in each clade. These predictions rely heavily on previous descriptions of the dietary ecology of these species, and particularly on available data regarding food material properties (e.g., Williams et al., 2005, Wright, 2005, Norconk et al., 2009).
Five ateline species were studied in the pairwise analysis: Ateles geoffroyi, Lagothrix lagothrica, and three species of Alouatta (Alouatta seniculus, Alouatta belzebul, and Alouatta palliata). Among these taxa, A. geoffroyi and L. lagothrica are the most frugivorous, consuming between 74% and 87% fruit parts in their diets (Chapman, 1987, Chapman, 1989, Peres, 1994, Di Fiore, 2004, Russo et al., 2005). These species differ, however, in their relative consumption of seeds and insect prey. Some data suggest that L. lagothrica is a seasonal seed predator and relies more heavily on insect parts than does A. geoffroyi (van Roosmalen and Klein, 1988, Peres, 1994, Di Fiore, 2004, Russo et al., 2005). In contrast, Alouatta is the most folivorous of all New World primates, although there is considerable variation in this group. A. seniculus consumes approximately 50% leaves, with a preference for young rather than mature leaves. The remainder of its diet is composed of fruit and flowers (Gaulin and Gaulin, 1982, Julliot, 1996). Food items opened or breached and/or masticated by Alouatta are substantially more resistant than those utilized by Ateles, both in average and maximum toughness (Wright, 2004, Norconk et al., 2009). No comparable data are available for Lagothrix. Another consideration in this clade is the highly derived nature of the vocal apparatus in Alouatta. Members of this genus are characterized by their distinctive vocal behaviors (e.g., Carpenter, 1934, Hershkovitz, 1949, Altmann, 1959), which could be associated with relatively larger gapes. However, no behavioral data quantifying gape during vocalizations in these species are currently available.
Morphological differences in the masticatory apparatus of the atelines have also been extensively evaluated. The more folivorous Alouatta exhibits relatively higher occlusal relief and relatively greater molar area compared with the more frugivorous Ateles and Lagothrix (Hylander, 1975, Kay, 1975, Rosenberger and Kinzey, 1976, Rosenberger and Strier, 1989, Anapol and Lee, 1994). Similarly, Alouatta has been argued to exhibit a more robust masticatory apparatus (e.g., high TMJ, robust mandible, larger temporal fossa) compared with Ateles (Rosenberger and Strier, 1989, Spencer, 1995).
Given the ecological and morphological data, when compared with the relatively more gracile Ateles, Alouatta should have relatively larger condylar joint surface areas because of their heavy reliance on tough food objects. Increased use of the postcanine dentition in Alouatta predicts a relatively mediolaterally wider joint as well. However, Alouatta is also predicted to have relatively anteroposteriorly longer joints to facilitate generating relatively wider jaw gapes during their distinctive vocal behaviors. Additionally, Alouatta is predicted to have the relatively highest entoglenoid process and articular tubercle to guide movements of the condyle during masticatory and/or vocal behaviors. In contrast, Lagothrix and Ateles should have relatively smaller joint surface areas and processes, and also have relatively shorter joints in the anteroposterior dimension.
Three species of Cebus (subfamily Cebinae) were included in this study: Cebus capucinus and Cebus albifrons (non-apelloids), and Cebus apella. Although primarily frugivorous, all three taxa consume vertebrates, invertebrates, leaves, and flowers to some extent (Izawa and Mizuno, 1977, Izawa, 1979, Freese and Oppenheimer, 1981, Chapman and Fedigan, 1990, Janson and Boinski, 1992). In addition, all three species use their anterior teeth during ingestive behaviors, including processing seeds (Terborgh, 1986, Janson and Boinski, 1992). However, C. apella exploits relatively greater amounts of resistant foods compared with the non-apelloid capuchins (Terborgh, 1983). In particular, C. apella spends a larger percentage of time feeding on Astrocaryum nuts, the hard outer husks of which require either manual preparation and/or dental preparation, often in the form of the use of the canines as a wedge to further propagate cracks (Izawa and Mizuno, 1977, Izawa, 1979, Terborgh, 1983, Janson and Boinski, 1992).
Numerous morphological analyses of cebine masticatory morphology are consistent with the finding that C. apella exploits tougher and stiffer food objects than non-apelloids, and that these relatively large food items necessitate wide jaw gapes (Kinzey, 1974, Rosenberger and Kinzey, 1976, Teaford, 1985, Bouvier, 1986b, Cole, 1992, Daegling, 1992, Spencer, 1995, Wright, 2005, Norconk et al., 2009, Taylor and Vinyard, 2009). Interestingly, Spencer (1995) and Wright (2005) examined variation in Cebus masticatory morphology in the context of Greaves’s (1978) model, with somewhat mixed results. Spencer (1995) did not find any consistent differences in masticatory configuration among species of Cebus and hypothesized instead that the ability of C. apella to utilize more resistant food objects was related to differences in soft tissue anatomy. In contrast, Wright (2005) found that the masticatory apparatus of C. apella was more advantageous for generating and dissipating higher masticatory forces (particularly along the anterior dentition) than other Cebus species, although these forces may be relatively infrequent.
Given these data, C. apella is expected to exhibit relatively larger condylar surface areas as a consequence of their assumed relatively larger joint reaction forces (Table 1). In addition, increased use of the anterior dentition and ingestion and biting of relatively large food objects along the postcanine dentition suggest C. apella should have a relatively anteroposteriorly longer glenoid and mandibular condyle, which should facilitate achieving the larger gapes necessary for food processing. This increased gape is also expected to be accompanied by a relatively large entoglenoid process that acts to guide the movement of the condyle and function to increase the joint surface area of the TMJ, as well as an enlarged articular tubercle.
Cacajao melanocephalus, Chiropotes satanas, and Pithecia pithecia are included from the subfamily Pitheciinae. All three species feed primarily on seeds, particularly when fruits are less available (Buchannon et al., 1981, van Roosmalen et al., 1981, van Roosmalen et al., 1988, Ayres, 1989, Kinzey, 1992, Boubli, 1999). Collectively, these three taxa have been identified as ‘sclerocarp harvesters’ (Kinzey, 1992). Kinzey (1992) noted that this type of foraging involves two distinct stages: initial removal of the hard outer husk of seeds with the anterior dentition, and mastication by the posterior dentition of the softer inner seed parts. The first part of this process requires the use of the pitheciine’s large wedge-shaped canines and procumbent incisors to open tough food items (van Roosmalen et al., 1988, Ayres, 1989, Kinzey, 1992). Of these taxa, Pithecia has been suggested to be the least specialized for seed predation, primarily because of its more generalized masticatory morphology, lower molar relief, and less well-developed canines (Kinzey, 1992, Kinzey and Norconk, 1993). Spencer (1995) tested the hypothesis that Pithecia was more generalized than either Chiropotes or Cacajao, and found that the mechanical advantage of the masticatory muscles in Pithecia was substantially lower than in Chiropotes and Cacajao. Additionally, Norconk et al. (2009) found that among pitheciines, the masticatory apparatus of Pithecia has the lowest mechanical advantage for biting on the anterior teeth. This may be associated with the greater proportion of leaves in the diet of Pithecia compared with Chiropotes and Cacajao. However, C. satanas and P. pithecia ingest and masticate foods of comparable average and maximum toughness, and in fact, Pithecia has been documented to breach food items that are considerably tougher than those processed by Chiropotes (Wright, 2004, Norconk et al., 2009).
These data suggest that Cacajao and Chiropotes should both have relatively larger condylar surface areas as a consequence of their increased reliance on seed predation (and therefore presumably larger joint reaction forces) (Table 1). Both of these taxa may also be expected to have relatively anteroposteriorly longer joint surface areas because of their extensive use of the anterior dentition. In contrast, Pithecia should have relatively mediolaterally wider joints with a larger articular tubercle and entoglenoid process as a result of their increased use of the postcanine dentition.
Section snippets
Materials and methods
To examine TMJ shape variation in the sample and to test the predictions, three-dimensional (3D) coordinate data describing the shape of the glenoid fossa and mandibular condyle were collected on females and males from 13 platyrrhine species (Table 2). Data were collected using a Microscribe G2X digitizer (Immersion Corp.). The measured accuracy for the Microscribe G2X is ±0.23 mm, and an analysis of intraobserver error for this dataset found an average error of approximately 0.03 mm for the
Platyrrhine TMJ variation
In the geometric morphometric analysis of the entire sample (Fig. 2), PC 1 separates the three Alouatta species from the rest of the sample. This PC explains 43% of the sample variance and is significantly correlated with size in females (r2 = 0.497, p = 0.007) and males (r2 = 0.680, p = 0.007). Shape variation along this axis is primarily associated with postglenoid process projection, and to a lesser degree, the relative anteroposterior and mediolateral dimensions of the joint. PC2 (which
TMJ size and shape variation across platyrrhines
Analysis of TMJ variation across the platyrrhine sample highlights the wide range of variation in glenoid shape present in this clade. Importantly, this analysis found a relationship between size and shape of the TMJ and diet, particularly when seeds and leaves are considered separately. Assuming that dietary categories bear some relationship to food material properties, the results of this study further suggest that differentiating between seeds and leaves may be important for understanding
Conclusions
The data presented here suggest mixed correlations between feeding behavior and the morphology of the TMJ in platyrrhine primates. The correlations observed among the shape, size, and dietary matrices suggest relationships among all of these datasets, and demonstrate that both size and diet are significant factors influencing TMJ morphology in New World primates. Analyses of 3D TMJ shape variation in each of the three comparative groups further indicated that some aspects of TMJ morphology can
Acknowledgments
Thanks go to all of the individuals and institutions that made collections available for this research: American Museum of Natural History, the Department of Primatology at the State Collection of Anthropology and Paleoantomy, the National Museum of Natural History, the Field Museum, and the Royal Museum for Central Africa. Valuable feedback was received from Bill Kimbel, Gary Schwartz, Mark Spencer, Andrea Taylor, Christine Wall, Chris Vinyard, David Begun and two anonymous reviewers. Any
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