Christopher J. Vinyard

ONTOGENY, FUNCTION, AND SCALING OF THE MANDIBULAR SYMPHYSIS IN PAPIONIN PRIMATES

In vivo study of mastication in adult cercopithecine primates demonstrates a link between mandibular symphyseal form and resistance to “wishboning,” or lateral transverse bending. Mechanical consideration of wishboning at the symphysis indicates exponentially higher stresses along the lingual surface with increasing symphyseal curvature. Lengthening the anteroposterior width of the symphysis acts to resist these higher loads. Interspecific adult cercopithecine allometries show that both symphyseal curvature and symphyseal width exhibit positive allometry relative to body mass. The experimental and allometric data support an hypothesis that the cercopithecine mandibular symphysis is designed to maintain functional equivalence—in this case dynamic strain similarity—in wishboning stress and strain magnitudes across adult cercopithecines.

Mechanical and Nutritional Properties of Food as Factors in Platyrrhine Dietary Adaptations

Platyrrhines face a vast array of potential food resources in the Neotropics. Ecological challenges associated with finding, ingesting, masticating, and digesting foods are influenced by food availability and accessibility. Food availability is influenced by seasonal variation in forest productivity, fruiting synchrony, and crop size (e.g., Stevenson 2001; Chapman et al. 2003, but see Milton et al. 2005). Accessibility, on the other hand, is related to such factors as fruit and seed size, the ability to breach mechanically challenging tissues, to tolerate secondary chemical compounds, and to balance nutrient intake. Our goal in this chapter is to examine the diversity of platyrrhine responses to this second variable – gaining access to and processing foods. All platyrrhine genera include fruit in their diets, but the annual percentage of fruit intake ranges widely from 8% in Cebuella to 86% in Ateles (Table 11.1). A wide variety of other resources including exudates, fungi, leaves, flowers, nectar and insect or vertebrate prey make up the balance, or at times the bulk, of annual diets. Some particularly interesting feeding behaviors seen in platyrrhines signal the evolution of specific adaptations. These include the ability to extract and digest plant resources such as gums by Cebuella and Callithrix (Nash 1986; Power and Oftedal 1996), fungi by Callimico (Porter 2001; Porter and Garber 2004; Hanson et al. 2006; Rehg 2006), and seeds by the pitheciins (van Roosmalen et al. 1988; Ayres 1989; Kinzey and Norconk 1990; Kinzey 1992; Peetz 2001; Norconk and Conklin-Brittain 2004). Although gums, seeds and fungi are ingested by other primate species [especially lemurs (Nash 1989; Hemingway 1998) and colobines (Waterman and Kool 1994; Kirkpatrick 1998)], they are used very intensively by these platyrrhines, composing either a majority of their diet during a single season, a subset of the annual diet, or are routinely and extensively used throughout the year.

Evolution of anthropoid jaw loading and kinematic patterns

Major transformations in the skull and masticatory system characterized the evolution of crown anthropoids. To offer further insight into the phylogenetic and arguably adaptive significance of specific primate mandibular loading and kinematic patterns, allometric analyses of metric parameters linked to masticatory function are performed within and between 47 strepsirhine and 45 recent anthropoid species. When possible, basal anthropoids are considered. These results are subsequently integrated with prior experimental and morphological work on primate skull form. As compared to strepsirhines, crown anthropoids have a vertically longer ascending ramus linked to a glenoid and condyle positioned relatively higher above the occlusal plane. Interestingly, anthropoids and strepsirhines do not exhibit different mean ratios of condylar to glenoid height, which suggests that both clades are similar in their ability to evenly distribute occlusal contacts and perhaps forces along the postcanine teeth. Thus, given the considerable suborder differences in the scaling of both glenoid and condylar height, we argue that much of this variation in jaw-joint height is linked to suborder differences in relative facial height due in turn to increased encephalization, basicranial flexion, and facial kyphosis in anthropoids. Due to a more elongate ascending ramus, anthropoids evince more vertically oriented masseters than like-sized strepsirhines. Having a relatively longer ramus and a more medially displaced lateral pterygoid plate, crown anthropoids exhibit medial pterygoids oriented similar to those of strepsirhines, but with a variably longer lever arm. As anthropoid masseters are less advantageously placed to effect transverse movements/forces, we argue that balancing-side deep-masseter activity underlying a wishboning loading regime serves to increase, or at least maintain, transverse levels of jaw movement and occlusal force at the end of the masticatory power stroke. Crown anthropoids are also more isognathic and isodontic than strepsirhines. A consideration of early anthropoids suggests that the crown anthropoid masticatory pattern, i.e., more vertical masseters due to a high condyle as well as greater isognathy and isodonty, occurred stepwise during stem anthropoid evolution. This appears to correspond to a more transverse, and perhaps progressively larger, power stroke across oligopithecids, parapithecids, and propliopithecids.

Food Oral Processing: Conversion of Food Structure to Textural Perception

Food oral processing includes all muscle activities, jaw movements, and tongue movements that contribute to preparing food for swallowing. Simultaneously, during the transformation of food structure to a bolus, a cognitive representation of food texture is formed. These physiological signals detected during oral processing are highly complex and dynamic in nature because food structure changes continuously due to mechanical and biochemical breakdown coupled with the lubricating action of saliva. Multiple and different sensations are perceived at different stages of the process. Although much work has focused on factors that determine mechanical (e.g., rheological and fracture) and sensory properties of foods, far less attention has been paid to linking food transformations that occur during oral processing with sensory perception of texture. Understanding how food structure influences specific patterns of oral processing and how these patterns relate to specific textural properties and their cognitive representations facilitates the design of foods that are nutritious, healthy, and enjoyable.

The Evolutionary Morphology of Tree Gouging in Marmosets

The marmosets, Callithrix spp. and Cebuella pygmaea, are unique among anthropoids in their habitual biting of trees with their anterior teeth to elicit exudate flow. This tree-gouging behavior is thought to offer certain ecological benefits to marmosets, such as routine access to an under-exploited resource, as well as have specific influences on their behavioral ecology.

The functional correlates of jaw‐muscle fiber architecture in tree‐gouging and nongouging callitrichid monkeys

Common (Callithrix jacchus) and pygmy (Cebuella pygmaea) marmosets and cotton-top tamarins (Saguinus oedipus) share broadly similar diets of fruits, insects, and tree exudates. Marmosets, however, differ from tamarins in actively gouging trees with their anterior dentition to elicit tree exudates flow. Tree gouging in common marmosets involves the generation of relatively wide jaw gapes, but not necessarily relatively large bite forces. We compared fiber architecture of the masseter and temporalis muscles in C. jacchus (N = 18), C. pygmaea (N = 5), and S. oedipus (N = 13). We tested the hypothesis that tree-gouging marmosets would exhibit relatively longer fibers and other architectural variables that facilitate muscle stretch. As an architectural trade-off between maximizing muscle excursion/contraction velocity and muscle force, we also tested the hypothesis that marmosets would exhibit relatively less pinnate fibers, smaller physiologic cross-sectional areas (PCSA), and lower priority indices (I) for force. As predicted, marmosets display relatively longer-fibered muscles, a higher ratio of fiber length to muscle mass, and a relatively greater potential excursion of the distal tendon attachments, all of which favor muscle stretch. Marmosets further display relatively smaller PCSAs and other features that reflect a reduced capacity for force generation. The longer fibers and attendant higher contraction velocities likely facilitate the production of relatively wide jaw gapes and the capacity to generate more power from their jaw muscles during gouging. The observed functional trade-off between muscle excursion/contraction velocity and muscle force suggests that primate jaw-muscle architecture reflects evolutionary changes related to jaw movements as one of a number of functional demands imposed on the masticatory apparatus.

Stressed Out: Masticatory Forces and Primate Circumorbital Form

Editor’s note: This pair of articles— Anat Rec (New Anat) 261:173–175 (Ravosa et al.) and 170–172 (Prossinger et al.), 2000—were originally submitted as a Letter to the Editor commenting on the article by Bookstein et al. [Anat Rec (New Anat) 257:217-224, 1999] and a Response by the Bookstein et al. (1999) authors. The Editorial Board concluded that the length and depth of this scientific discussion on one aspect of the referenced article—viz., possible relationships between browridge morphology and masticatory stress in ancient vs. modern hominids—warranted more space than is typically offered to Letters to the Editor. We therefore decided to publish these articles back to back, as brief Point/Counterpoint articles, in order to let the researcher present well-developed arguments on both sides of this intriguing debate. The authors of Bookstein et al. (1999) recently employed a suite of imaging techniques and morphometric analyses to describe evolutionary changes in circumorbital form among Pleistocene hominids. In discussing the broader implications of their study, they claim that, contrary to specific in vivo (Hylander et al., 1991a) and comparative (Ravosa, 1991b) work, “the external form of the browridges is related to the need to resolve the stresses in the face. . . induced by mastication” (Bookstein et al., 1999; p. 222). This conclusion is based on “the inner morphology of the frontal sinuses in the CT scans” of various hominoid crania, specifically the thin “anterior and posterior walls of the sinuses” (Bookstein et al., 1999; p. 222). According to the authors, “thinning minimizes bone mass without compromising the necessary strength, suggesting that. . .externally enormous supraorbital structures do relate to masticatory stresses” (Bookstein et al., 1999; p. 222). The purpose of our response is threefold. First, we address their argument regarding the functional significance of thin-walled browridges. Second, we indicate that recent in vivo bone-strain analyses provide no support for any masticatory-stress hypothesis of circumorbital form. Third, based on experimental and morphological data, we show that, rather than being adapted to counter masticatory stresses, variation in browridge proportions and frontal sinus pneumatization is supportive of the spatial model of supraorbital torus formation (Moss and Young, 1960; Shea, 1986; Ravosa, 1988, 1991a,b; Hylander and Ravosa, 1992). If Bookstein et al. (1999) insist that a thin-walled supraorbital torus in humans is especially designed for resisting masticatory stresses, we should then ask what kind of evidence would support a refutation of this hypothesis. Presumably the presence of a thicker-walled supraorbital torus would constitute such a refutation. But this does not seem reasonable since we could just as easily argue that relatively thicker walls also represent an adaptation to larger routine masticatory forces. This dilemma highlights the inherent difficulty in evaluating the functional significance of skull form in the absence of experimental data. This is perhaps best underscored by the lesson of the macaque zygomatic arch. In this primate, the thin cortical bone of the posterior region of the arch experiences very low strains, whereas the thick cortical bone of the anterior portion is a high strain area (Hylander and Johnson, 1997). Such a pattern is opposite to what would be predicted if Bookstein et al.’s (1999) morphological criterion were the sole means of inferring browridge function. Thus, we argue that the data employed by Bookstein et al. can provide neither support for, nor a refutation of, their claim regarding the masticatory determinants of variation in the thickDr. Ravosa is an associate professor in the Dept. of Cell and Molecular Biology at Northwestern University Medical School, and a research associate in the Dept. of Zoology, Mammals Division, at the Field Museum of Natural History. He is interested in the biomechanics, development, and ecomorphology of the mammalian skull, particularly as it relates to major morphological transformations during the origin of higher clades. Dr. Vinyard is a research associate, and Dr. Hylander is a professor, in the Dept. of Biological Anthropology and Anatomy at Duke University Medical Center. Dr. Vinyard is interested in morphological integration in the primate skull, and how covariation in craniofacial structures is related to the functional morphology and evolutionary history of this anatomical complex. Dr. Hylander studies the functional morphology and biomechanics of the vertebrate cranium, especially in primates. Over the past 25 years his laboratory has pioneered the development and application of in vivo bone-strain and jawmuscle EMG investigations of the masticatory apparatus. *Correspondence to: Dr. Matthew J. Ravosa, Department of Cell and Molecular Biology, Northwestern University Medical School, 303 East Chicago Ave, Chicago IL 60611-3008 USA. Fax: 312-503-7912; E-mail: m-ravosa@northwestern.edu THE ANATOMICAL RECORD (NEW ANAT.) 261:173–175, 2000

Cross-sectional Bone Distribution in the Mandibles of Gouging and Non-gouging Platyrrhini

Recent morphometric analyses have led to dissimilar conclusions about whether the jaws of tree-gouging primates are designed to resist the purportedly large forces generated during this biting behavior. We further address this question by comparing the cross-sectional geometry of the mandibular corpus and symphysis in tree-gouging common marmosets (Callithrix jacchus) to nongouging saddleback tamarins (Saguinus fuscicollis) and squirrel monkeys (Saimiri sciureus). As might be expected, based on size, squirrel monkeys tend to have absolutely larger cross-sectional areas at each tooth location sampled, while saddleback tamarins are intermediate, followed by the smaller common marmosets. Similarly, the amount and distribution of cortical bone in squirrel monkey jaws provides them with increased ability to resist sagittal bending (Ixx) and torsion (K) in the corpus as well as coronal bending (Ixx) and shearing in the symphysis. However, when the biomechanical parameters are scaled to respective load arm estimates, there are few significant differences in relative resistance abilities among the 3 species. A power analysis indicates that we cannot statistically rule out subtle changes in marmoset jaw form linked to resisting loads during gouging. Nevertheless, our results correspond to studies in vivo of jaw loading, field data, and other comparative analyses suggesting that common marmosets do not generate relatively large bite forces during tree gouging. The 3 species are like most other anthropoids in having thinner bone on the lingual than on the buccal side of the mandibular corpus at M1. The similarity in corporal shape across anthropoids supports a hypothesized stereotypical pattern of jaw loading during chewing and may indicate a conserved pattern of mandibular growth for the suborder. Despite the overall similarity, platyrrhines may differ slightly from catarrhines in the details of their cortical bone distribution.

A Biomechanical Analysis of Skull Form in Gum-Harvesting Galagids

Among primates, some highly gummivorous species habitually gouge trees to elicit exudate flow whereas others scrape the hardened gums from trees. These foraging behaviors are thought to require high external forces at the anterior dentition. In this study, we test whether skull form in gouging and scraping galagids corresponds to this suggested need to produce these higher external forces and to resist increased internal loads in the jaws. We find few consistent morphological patterns linking skull form and the generation of high forces during gouging. However, there is some tendency for gougers and scrapers to show increased load resistance capabilities in their mandibles. Future research on the mechanical properties of trees exploited by these species and on jaw function during gouging and scraping will improve our understanding of the mechanical demands of gum feeding on the galagid skull form.

Linking Laboratory and Field Approaches in Studying the Evolutionary Physiology of Biting in Bamboo Lemurs

A realistic understanding of primate morphological adaptations requires a multidisciplinary approach including experimental studies of physiological performance and field studies documenting natural behaviors and reproductive success. For primate feeding, integrative efforts combining experimental and ecological approaches are rare. We discuss methods for collecting maximum bite forces in the field as part of an integrated ecomorphological research design. Specifically, we compare maximum biting ability in 3 sympatric bamboo lemurs (Hapalemur simus, H. aureus, and H. griseus) at Ranomafana National Park, Madagascar to determine if biting performance contributes to the observed partitioning of a shared bamboo diet. We assessed performance by recording maximum bite forces via jaw-muscle stimulations in anesthetized subjects from each species. Behavioral observations and food properties testing show that the largest species, Hapalemur simus, consumes the largest and most mechanically challenging foods. Our results suggest that Hapalemur simus can generate larger bite forces on average than those of the 2 smaller species. However, the overlap in maximum biting ability between Hapalemur simus and H. aureus indicates that biting performance cannot be the sole factor driving dietary segregation. Though maximum bite force does not fully explain dietary segregation, we hypothesize that size-related increases in both maximum bite force and jaw robusticity provide Hapalemur simus with an improved ability to process routinely its more obdurate diet. We demonstrate the feasibility of collecting physiological, ecological, and morphological data on the same free-ranging primates in their natural habitats. Integrating traditionally laboratory-based approaches with field studies broadens the range of potential primate species for physiological research and fosters improved tests of hypothesized feeding adaptations.