Publications

2011

Vinyard, Christopher J, Andrea B Taylor, Mark F Teaford, Kenneth E Glander, Matthew J Ravosa, James B Rossie, Timothy M Ryan, and Susan H Williams. (2011) 2011. “Are We Looking for Loads in All the Right Places? New Research Directions for Studying the Masticatory Apparatus of New World Monkeys.”. Anatomical Record (Hoboken, N.J. : 2007) 294 (12): 2140-57. https://doi.org/10.1002/ar.21512.

New World monkeys display a wide range of masticatory apparatus morphologies related to their diverse diets and feeding strategies. While primatologists have completed many studies of the platyrrhine masticatory apparatus, particularly morphometric analyses, we collectively acknowledge key shortcomings in our understanding of the function and evolution of the platyrrhine feeding apparatus. Our goal in this contribution is to review several recent, and in most cases ongoing, efforts to address some of the deficits in our knowledge of how the platyrrhine skull is loaded during feeding. We specifically consider three broad research areas: (1) in vivo physiological studies documenting mandibular bone strains during feeding, (2) metric analyses assessing musculoskeletal functional morphology and performance, as well as (3) the initiation of a physiological ecology of feeding that measures in vivo masticatory mechanics in a natural environment. We draw several conclusions from these brief reviews. First, we need better documentation of in vivo strain patterns in the platyrrhine skull during feeding given their empirical role in developing adaptive hypotheses explaining masticatory apparatus form. Second, the greater accuracy of new technologies, such as CT scanning, will allow us to better describe the functional consequences of jaw form. Third, performance studies are generally lacking for platyrrhine jaws, muscles, and teeth and offer exciting avenues for linking form to feeding behavior and diet. Finally, attempts to bridge distinct research agendas, such as collecting in vivo physiological data during feeding in natural environments, present some of the greatest opportunities for novel insights into platyrrhine feeding biology.

2010

Williams, Susan H, JoAnna Sidote, and Kristin K Stover. (2025) 2010. “Occlusal Development and Masseter Activity in Alpacas (Lama Pacos)”. Anatomical Record (Hoboken, N.J. : 2007) 293 (1): 126—134. https://doi.org/10.1002/ar.21016.
Tooth eruption and the development of occlusion are significant ontogenetic changes in the masticatory apparatus of mammals. Here, we test the hypothesis that changes in masseter activity are correlated with increased occlusal contacts at major stages of dental development in the alpaca, Lama pacos. We compare electromyographic data from the superficial and deep masseter in infant and juvenile alpacas prior to and following m1 occlusion and from adults with full permanent dentitions. The pre-m1 and post-m1 occlusion groups exhibit similar masseter activity durations, chewing cycle durations, and with the exception of the balancing-side deep masseter, similar timing differences between the jaw muscles. On average, the balancing-side deep masseter fires significantly later in the post-m1 occlusion group. The m2-m3 group exhibits significantly longer chewing cycle length and an even later firing balancing-side deep masseter. Increased occlusion is also associated with an increase in the relative amount of working-side superficial and deep masseter muscle activity when compared with the balancing side muscles. Although the development of occlusal relations in infant and juvenile alpacas are associated with minor changes in masseter activation patterns, additional molar occlusal contacts increase chewing cycle duration resulting in concomitant changes in masseter recruitment patterns. Currently, we cannot rule out that musculoskeletal development influences masseter activity as demonstrated in other mammals. However, the data presented here indicate that alpacas have a relatively delayed onset of the adult motor pattern that may be correlated with changes in occlusal relations due to tooth eruption.
Ravosa, Matthew J, Callum F Ross, Susan H Williams, and Destiny B Costley. (2025) 2010. “Allometry of Masticatory Loading Parameters in Mammals”. Anatomical Record (Hoboken, N.J. : 2007) 293 (4): 557—571. https://doi.org/10.1002/ar.21133.
Considerable research on the scaling of loading patterns in mammalian locomotor systems has not been accompanied by a similarly comprehensive analysis of the interspecific scaling of loading regimes in the mammalian masticatory complex. To address this deficiency, we analyzed mandibular corpus bone strain in 11 mammalian taxa varying in body size by over 2.5 orders of magnitude, including goats, horses, alpacas, pigs, and seven primate taxa. During alert chewing and biting of hard/tough foods, bone-strain data were collected with rosette gauges placed along the lateral aspect of the mandibular corpus below the molars or premolars. Bone-strain data were used to characterize relevant masticatory loading parameters: peak loading magnitudes, chewing cycle duration, chewing frequency, occlusal duty factor, loading rate, and loading time. Interspecific analyses indicate that much as observed in limb elements, corpus peak-strain magnitudes are similar across mammals of disparate body sizes. Chewing frequency is inversely correlated with body size, much as with locomotor stride frequency. Some of this allometric variation in chewing frequency appears to be due to a negative correlation with loading time, which increases with body size. Similar to the locomotor apparatus, occlusal duty factor, or the duration of the chewing cycle during which the corpus is loaded, does not vary with body size. Peak principal-strain magnitudes are most strongly positively correlated with loading rate and only secondarily with loading, with this complex relationship best described by a multiple regression equation with an interaction term between loading rate and loading time. In addition to informing interpretations of craniomandibular growth, form, function, and allometry, these comparisons provide a skeleton-wide perspective on the patterning of osteogenic stimuli across body sizes.
Davis, Jillian S, Christopher W Nicolay, and Susan H Williams. (2010) 2010. “A Comparative Study of Incisor Procumbency and Mandibular Morphology in Vampire Bats.”. Journal of Morphology 271 (7): 853-62. https://doi.org/10.1002/jmor.10840.

The three species of vampire bats (Phyllostomidae: Desmodontinae), Desmodus rotundus, Diaemus youngi, and Diphylla ecaudata, are the only mammals that obtain all nutrition from vertebrate blood (sanguinivory). Because of the unique challenges of this dietary niche, vampire bats possess a suite of behavioral, physiological, and morphological specializations. Morphological specializations include a dentition characterized by small, bladelike, non-occlusive cheek teeth, large canines, and extremely large, procumbent, sickle-shaped upper central incisors. The tips of these incisors rest in cuplike pits in the mandible behind the lower incisors (mandibular pits). Here, we use microCT scanning and high-resolution radiography to describe the morphology of the mandible and anterior dentition in vampire bats, focusing on the relationship between symphyseal fusion, mandibular pit size, incisor size, and procumbency. In Desmodus and Diaemus, highly procumbent upper incisors are associated with relatively small mandibular pits, an unfused mandibular symphysis with substantial bony interdigitations linking the dentaries, and a diastema between the lower central incisors that helps to facilitate the lapping of blood from a wound. In Diphylla, less procumbent upper incisors are associated with relatively large mandibular pits, a completely fused mandibular symphysis, and a continuous lower toothrow lacking a central diastema. We hypothesize that symphyseal morphology and the presence or absence of the diastema are associated with the angle of upper incisor procumbency and mandibular pit development, and that spatial constraints influence the morphology of the symphysis. Finally, this morphological variation suggests that Diphylla utilizes a different feeding strategy as compared to Desmodus and Diaemus, possibly resulting from the functional demands of specialization on avian, rather than mammalian, blood.

2009

Williams, Susan H, Christopher J Vinyard, Christine E Wall, and William L Hylander. (2025) 2009. “Mandibular Corpus Bone Strain in Goats and Alpacas: Implications for Understanding the Biomechanics of Mandibular Form in Selenodont Artiodactyls”. Journal of Anatomy 214 (1): 65—78. https://doi.org/10.1111/j.1469-7580.2008.01008.x.
The goal of this study is to clarify the functional and biomechanical relationship between jaw morphology and in vivo masticatory loading in selenodont artiodactyls. We compare in vivo strains from the mandibular corpus of goats and alpacas to predicted strain patterns derived from biomechanical models for mandibular corpus loading during mastication. Peak shear strains in both species average 600-700 microepsilon on the working side and approximately 450 microepsilon on the balancing side. Maximum principal tension in goats and alpacas is directed at approximately 30 degrees dorsocaudally relative to the long axis of the corpus on the working side and approximately perpendicular to the long axis on the balancing side. Strain patterns in both species indicate primarily torsion of the working-side corpus about the long axis and parasagittal bending and/or lateral transverse bending of the balancing-side corpus. Interpretation of the strain patterns is consistent with comparative biomechanical analyses of jaw morphology suggesting that in goats, the balancing-side mandibular corpus is parasagittally bent whereas in alpacas it experiences lateral transverse bending. However, in light of higher working-side corpus strains, biomechanical explanations of mandibular form also need to consider that torsion influences relative corpus size and shape. Furthermore, the complex combination of loads that occur along the selenodont artiodactyl mandibular corpus during the power stroke has two implications. First, added clarification of these loading patterns requires in vivo approaches for elucidating biomechanical links between mandibular corpus morphology and masticatory loading. Second, morphometric approaches may be limited in their ability to accurately infer masticatory loading regimes of selenodont artiodactyl jaws.
Williams, Susan H, Erika Peiffer, and Sonya Ford. (2025) 2009. “Gape and Bite Force in the Rodents Onychomys Leucogaster and Peromyscus Maniculatus: Does Jaw-Muscle Anatomy Predict Performance?”. Journal of Morphology 270 (11): 1338—1347. https://doi.org/10.1002/jmor.10761.
Compared with the deer mouse, Peromyscus maniculatus, the grasshopper mouse, Onychomys leucogaster, exhibits modifications in its jaw-muscle architecture that promote wide gapes and large bite forces at wide gapes to prey upon large vertebrate prey. In this study, we determine whether jaw-muscle anatomy predicts gape and biting performance in O. leucogaster, and we also assess the influence of gape on bite force in the two species. Although O. leucogaster has an absolutely longer jaw, which facilitates larger gapes, maximum passive gape is similar in both species, averaging approximately 12.5 mm. Thus, when scaled to jaw length, O. leucogaster has a smaller maximum passive gape. These results suggest that predatory behaviors of O. leucogaster may not require remarkably large gapes. On the other hand, both absolute and relative bite forces exerted by O. leucogaster are significantly larger than those of P. maniculatus. The largest bite forces in both species occur at 5.0 mm of gape at the incisors, or 40% of maximum gape. Although bite force in both species decreases at larger gapes, O. leucogaster does maintain a larger percentage of maximum bite force at gapes larger than 40% of maximum passive gape. Therefore, although structural modifications in the masticatory apparatus of O. leucogaster may constrain gape, they may help to maintain bite force at large gapes. These results suggest that increases in gape differentially influence the length-tension properties of the jaw muscles in the two species. Finally, these results highlight the importance of considering the effect of muscle stretch on force production in comparative studies of bite force. As a first approximation, it appears that gapes of 40-50% of maximum gape in rodents optimizes bite force production at the incisors.

2008

Vinyard, Christopher J, Christine E Wall, Susan H Williams, and William L Hylander. (2025) 2008. “Patterns of Variation across Primates in Jaw-Muscle Electromyography During Mastication”. Integrative and Comparative Biology 48 (2): 294—311. https://doi.org/10.1093/icb/icn071.
Biologists that study mammals continue to discuss the evolution of and functional variation in jaw-muscle activity during chewing. A major barrier to addressing these issues is collecting sufficient in vivo data to adequately capture neuromuscular variation in a clade. We combine data on jaw-muscle electromyography (EMG) collected during mastication from 14 species of primates and one of treeshrews to assess patterns of neuromuscular variation in primates. All data were collected and analyzed using the same methods. We examine the variance components for EMG parameters using a nested ANOVA design across successive hierarchical factors from chewing cycle through species for eight locations in the masseter and temporalis muscles. Variation in jaw-muscle EMGs was not distributed equally across hierarchical levels. The timing of peak EMG activity showed the largest variance components among chewing cycles. Relative levels of recruitment of jaw muscles showed the largest variance components among chewing sequences and cycles. We attribute variation among chewing cycles to (1) changes in food properties throughout the chewing sequence, (2) variation in bite location, and (3) the multiple ways jaw muscles can produce submaximal bite forces. We hypothesize that variation among chewing sequences is primarily related to variation in properties of food. The significant proportion of variation in EMGs potentially linked to food properties suggests that experimental biologists must pay close attention to foods given to research subjects in laboratory-based studies of feeding. The jaw muscles exhibit markedly different variance components among species suggesting that primate jaw muscles have evolved as distinct functional units. The balancing-side deep masseter (BDM) exhibits the most variation among species. This observation supports previous hypotheses linking variation in the timing and activation of the BDM to symphyseal fusion in anthropoid primates and in strepsirrhines with robust symphyses. The working-side anterior temporalis shows a contrasting pattern with little variation in timing and relative activation across primates. The consistent recruitment of this muscle suggests that primates have maintained their ability to produce vertical jaw movements and force in contrast to the evolutionary changes in transverse occlusal forces driven by the varying patterns of activation in the BDM.

2007

Ross, Callum F, Alison Eckhardt, Anthony Herrel, William L Hylander, Keith A Metzger, Vicky Schaerlaeken, Rhyan L Washington, and Susan H Williams. (2025) 2007. “Modulation of Intra-Oral Processing in Mammals and Lepidosaurs”. Integrative and Comparative Biology 47 (1): 118—136. https://doi.org/10.1093/icb/icm044.
The mammalian masticatory apparatus is distinguished from the intra-oral processing systems of other amniotes by a number of morphological and functional features, including transverse movements of the teeth during the power stroke, precise occlusion, suspension of the teeth in the socket by a periodontal ligament, diphyodonty (reduction to two generations of teeth), a hard palate, and the presence of a single bone (the dentary) in the lower jaw which articulates with the skull at the temporomandibular jaw joint. The evolution of these features is commonly argued to have improved the efficiency of food processing in the oral cavity. The present aricle highlights the existence in mammals of the fusimotor system and afferent fibers from the periodontal ligament through which the CNS modulates the responses by the muscle spindles. Published data suggest that the fusimotor system and the periodontal afferents are important components in feed-forward (or anticipatory) control of chewing behavior. We hypothesize that this feed-forward control is used to maintain relatively constant cycle lengths in mammals in the face of intra-sequence and inter-sequence variation in material properties of the food, and that this enables them to maintain a higher average chewing frequency than that of lizards. These predictions were evaluated using data on mean cycle length and its variance from the literature and from our own files. On average, mammals have less variable cycle lengths than do lizards and shorter cycle lengths than do lizards of similar size. We hypothesize that by decreasing variance in cycle length, presumably close to the natural frequency of their feeding systems, mammals minimize energy expenditure during chewing, allowing them to chew for longer, thereby maintaining the high rates of food intake required for their high metabolic rates.
Ross, Callum F, Ruchi Dharia, Susan W Herring, William L Hylander, Zi-Jun Liu, Katherine L Rafferty, Matthew J Ravosa, and Susan H Williams. (2025) 2007. “Modulation of Mandibular Loading and Bite Force in Mammals During Mastication”. The Journal of Experimental Biology 210 (Pt 6): 1046—1063. https://doi.org/10.1242/jeb.02733.
Modulation of force during mammalian mastication provides insight into force modulation in rhythmic, cyclic behaviors. This study uses in vivo bone strain data from the mandibular corpus to test two hypotheses regarding bite force modulation during rhythmic mastication in mammals: (1) that bite force is modulated by varying the duration of force production, or (2) that bite force is modulated by varying the rate at which force is produced. The data sample consists of rosette strain data from 40 experiments on 11 species of mammals, including six primate genera and four nonprimate species: goats, pigs, horses and alpacas. Bivariate correlation and multiple regression methods are used to assess relationships between maximum (epsilon(1)) and minimum (epsilon(2)) principal strain magnitudes and the following variables: loading time and mean loading rate from 5% of peak to peak strain, unloading time and mean unloading rate from peak to 5% of peak strain, chew cycle duration, and chew duty factor. Bivariate correlations reveal that in the majority of experiments strain magnitudes are significantly (P0.001) correlated with strain loading and unloading rates and not with strain loading and unloading times. In those cases when strain magnitudes are also correlated with loading times, strain magnitudes are more highly correlated with loading rate than loading time. Multiple regression analyses reveal that variation in strain magnitude is best explained by variation in loading rate. Loading time and related temporal variables (such as overall chew cycle time and chew duty factor) do not explain significant amounts of additional variance. Few and only weak correlations were found between strain magnitude and chew cycle time and chew duty factor. These data suggest that bite force modulation during rhythmic mastication in mammals is mainly achieved by modulating the rate at which force is generated within a chew cycle, and less so by varying temporal parameters. Rate modulation rather than time modulation may allow rhythmic mastication to proceed at a relatively constant frequency, simplifying motor control computation.
Ross, Callum F, Alison Eckhardt, Anthony Herrel, William L Hylander, Keith A Metzger, Vicky Schaerlaeken, Rhyan L Washington, and Susan H Williams. (2007) 2007. “Modulation of Intra-Oral Processing in Mammals and Lepidosaurs.”. Integrative and Comparative Biology 47 (1): 118-36.

The mammalian masticatory apparatus is distinguished from the intra-oral processing systems of other amniotes by a number of morphological and functional features, including transverse movements of the teeth during the power stroke, precise occlusion, suspension of the teeth in the socket by a periodontal ligament, diphyodonty (reduction to two generations of teeth), a hard palate, and the presence of a single bone (the dentary) in the lower jaw which articulates with the skull at the temporomandibular jaw joint. The evolution of these features is commonly argued to have improved the efficiency of food processing in the oral cavity. The present aricle highlights the existence in mammals of the fusimotor system and afferent fibers from the periodontal ligament through which the CNS modulates the responses by the muscle spindles. Published data suggest that the fusimotor system and the periodontal afferents are important components in feed-forward (or anticipatory) control of chewing behavior. We hypothesize that this feed-forward control is used to maintain relatively constant cycle lengths in mammals in the face of intra-sequence and inter-sequence variation in material properties of the food, and that this enables them to maintain a higher average chewing frequency than that of lizards. These predictions were evaluated using data on mean cycle length and its variance from the literature and from our own files. On average, mammals have less variable cycle lengths than do lizards and shorter cycle lengths than do lizards of similar size. We hypothesize that by decreasing variance in cycle length, presumably close to the natural frequency of their feeding systems, mammals minimize energy expenditure during chewing, allowing them to chew for longer, thereby maintaining the high rates of food intake required for their high metabolic rates.