Tooth root morphology as an indicator for dietary specialization in carnivores (Mammalia: Carnivora)

The Carnivora occupy a wide range of feeding niches in concordance with the enormous diversity in their skull and dental form. It is well established that differences in crown morphology are linked to variations in the material properties of the foods ingested and masticated. However, how tooth root form is related to dietary specialization is less well known. In the present study, we investigate the relationship between tooth root morphology and dietary specialization in terrestrial carnivores (canids, felids, hyaenids, and ursids). We specifically address the question of how variation in tooth root surface area is related to bite force potentials as one of the crucial masticatory performance parameters in feeding ecology. We applied computed tomography imaging to reconstruct and quantify dental root surface area in 17 extant carnivore species. Moreover, we computed maximal bite force at several tooth positions based on a dry skull model and assessed the relationship of root surface area to skull size, maximal bite force, food properties, and prey size. We found that postcanine tooth root surface areas corrected for skull size serve as a proxy for bite force potentials and, by extension, dietary specialization in carnivores. Irrespective of taxonomic affinity, species that feed on hard food objects have larger tooth roots than those that eat soft or tough foods. Moreover, carnivores that prey on large animals have larger tooth root surface areas. Our results show that tooth root morphology is a useful indicator of bite force production and allows inferences to be made about dietary ecology in both extant and extinct mammals. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 456–471.     

Tooth chipping can reveal the diet and bite forces of fossil hominins

Mammalian tooth enamel is often chipped, providing clear evidence for localized contacts with large hard food objects. Here, we apply a simple fracture equation to estimate peak bite forces directly from chip size. Many fossil hominins exhibit antemortem chips on their posterior teeth, indicating their use of high bite forces. The inference that these species must have consumed large hard foods such as seeds is supported by the occurrence of similar chips among known modern-day seed predators such as orangutans and peccaries. The existence of tooth chip signatures also provides a way of identifying the consumption of rarely eaten foods that dental microwear and isotopic analysis are unlikely to detect.     

Food material properties and mandibular load resistance abilities in large-bodied hominoids

Numerous comparative studies have sought to demonstrate a functional link between feeding behavior, diet, and mandibular form in primates. In lieu of data on the material properties of foods ingested and masticated, many investigators have relied on qualitative dietary classifications such as "folivore" or "frugivore." Here we provide the first analysis of the relationship between jaw form, dietary profiles, and food material properties in large-bodied hominoids. We employed ratios of area moments of inertia and condylar area to estimate moments imposed on the mandible in order to evaluate and compare the relative ability to counter mandibular loads among central Bornean orangutans (Pongo pygmaeus wurmbii), Virunga mountain gorillas (Gorilla beringei beringei), and east African chimpanzees (Pan troglodytes schweinfurthii). We used data on elastic modulus (E) of fruit, fracture toughness (R) of fruit, leaves, and non-fruit, non-leaf vegetation, and derived fragmentation indices ( radicalR/E and radicalER), as proxies for bite force. We generated bending and twisting moments (forcexmoment arm) for various mandibular loading behaviors using food material properties to estimate minimally required bite forces. Based on E and R of foods ingested and masticated, we hypothesized improved resistance to mandibular loads in Pongo p. wurmbii compared to the African apes, and in G. b. beringei compared to Pan t. schweinfurthii. Results reveal that our predictions are borne out only when bite forces are estimated from maximum R of non-fruit, non-leaf vegetation. For all other tissues and material properties results were contrary to our predictions. Importantly, as food material properties change, the moments imposed on the mandible change; this, in turn, alters the entire ratio of relative load resistance to moment. The net effect is that species appear over- or under-designed for the moments imposed on the mandible. Our hypothesis, therefore, is supported only if we accept that maximum R of these vegetative tissues represents the relevant mechanical property influencing the magnitude of neuromuscular activity, food fragmentation, and mandibular morphology. A general implication is that reliable estimates of average and maximum bite forces from food material properties require that the full range of tissues masticated be tested. Synthesizing data on ingestive and masticatory behaviors, the number of chewing cycles associated with a given food, and food mechanical properties, should inform the broader question of which foods and feeding behaviors are most influential on the mandibular loading environment.     

Measuring the Toughness of Primate Foods and its Ecological Value

The mechanical properties of plant foods play an important role in the feeding process, being one of many criteria for food acceptance or rejection by primates. One of the simplest justifications for this statement is the general finding that primates tend to avoid foods with high fiber. Although fiber is largely tasteless, odorless, and colorless, it imparts texture, a sensation in the mouth related to the physical properties of foods. All primates encounter such mechanical resistance when they bite into plant food, and studies on humans show that an incisal bite facilitates quick oral assessment of a property called toughness. Thus, it is feasible that primates make similar assessments of quality in this manner. Here, we review methods of measuring the toughness of primate foods, which can be used either for making general surveys of the properties of foods available to primates or for establishing the mechanisms that protect these foods from the evolved form of the dentition.     

Indentation as a technique to assess the mechanical properties of fallback foods

A number of living primates feed part-year on seemingly hard food objects as a fallback. We ask here how hardness can be quantified and how this can help understand primate feeding ecology. We report a simple indentation methodology for quantifying hardness, elastic modulus, and toughness in the sense that materials scientists would define them. Suggested categories of fallback foods—nuts, seeds, and root vegetables—were tested, with accuracy checked on standard materials with known properties by the same means. Results were generally consistent, but the moduli of root vegetables were overestimated here. All these properties are important components of what fieldworkers mean by hardness and help understand how food properties influence primate behavior. Hardness sensu stricto determines whether foods leave permanent marks on tooth tissues when they are bitten on. The force at which a food plastically deforms can be estimated from hardness and modulus. When fallback foods are bilayered, consisting of a nutritious core protected by a hard outer coat, it is possible to predict their failure force from the toughness and modulus of the outer coat, and the modulus of the enclosed core. These forces can be high and bite forces may be maximized in fallback food consumption. Expanding the context, the same equation for the failure force for a bilayered solid can be applied to teeth. This analysis predicts that blunt cusps and thick enamel will indeed help to sustain the integrity of teeth against contacts with these foods up to high loads. Am J Phys Anthropol 140:643–652, 2009. © 2009 Wiley-Liss, Inc.     

Dietary hardness, loading behavior, and the evolution of skull form in bats

The morphology and biomechanics of the vertebrate skull reflect the physical properties of diet and behaviors used in food acquisition and processing. We use phyllostomid bats, the most diverse mammalian dietary radiation, to investigate if and how changes in dietary hardness and loading behaviors during feeding shaped the evolution of skull morphology and biomechanics. When selective regimes of food hardness are modeled, we found that species consuming harder foods have evolved skull shapes that allow for more efficient bite force production. These species have shorter skulls and a greater reliance on the temporalis muscle, both of which contribute to a higher mechanical advantage at an intermediate gape angle. The evolution of cranial morphology and biomechanics also appears to be related to loading behaviors. Evolutionary changes in skull shape and the relative role of the temporalis and masseter in generating bite force are correlated with changes in the use of torsional and bending loading behaviors. Functional equivalence appears to have evolved independently among three lineages of species that feed on liquids and are not obviously morphologically similar. These trends in cranial morphology and biomechanics provide insights into behavioral and ecological factors shaping the skull of a trophically diverse clade of mammals.     

Patterns of variation across primates in jaw-muscle electromyography during mastication

Biologists that study mammals continue to discuss the evolutionof and functional variation in jaw-muscle activity during chewing.A major barrier to addressing these issues is collecting sufficientin vivo data to adequately capture neuromuscular variation ina clade. We combine data on jaw-muscle electromyography (EMG)collected during mastication from 14 species of primates andone of treeshrews to assess patterns of neuromuscular variationin primates. All data were collected and analyzed using thesame methods. We examine the variance components for EMG parametersusing a nested ANOVA design across successive hierarchical factorsfrom chewing cycle through species for eight locations in themasseter and temporalis muscles. Variation in jaw-muscle EMGswas not distributed equally across hierarchical levels. Thetiming of peak EMG activity showed the largest variance componentsamong chewing cycles. Relative levels of recruitment of jawmuscles showed the largest variance components among chewingsequences and cycles. We attribute variation among chewing cyclesto (1) changes in food properties throughout the chewing sequence,(2) variation in bite location, and (3) the multiple ways jawmuscles can produce submaximal bite forces. We hypothesize thatvariation among chewing sequences is primarily related to variationin properties of food. The significant proportion of variationin EMGs potentially linked to food properties suggests thatexperimental biologists must pay close attention to foods givento research subjects in laboratory-based studies of feeding.The jaw muscles exhibit markedly different variance componentsamong species suggesting that primate jaw muscles have evolvedas distinct functional units. The balancing-side deep masseter(BDM) exhibits the most variation among species. This observationsupports previous hypotheses linking variation in the timingand activation of the BDM to symphyseal fusion in anthropoidprimates and in strepsirrhines with robust symphyses. The working-sideanterior temporalis shows a contrasting pattern with littlevariation in timing and relative activation across primates.The consistent recruitment of this muscle suggests that primateshave maintained their ability to produce vertical jaw movementsand force in contrast to the evolutionary changes in transverseocclusal forces driven by the varying patterns of activationin the BDM.     

Characterization of Food Physical Properties by the Mastication Parameters Measured by Electromyography of the Jaw-Closing Muscles and Mandibular Kinematics in Young Adults

The relationship between the physical properties of solid food and the masticatory parameters is clarified. Eight solid foods of varying physical properties were chosen. Electromyography of the jaw-closing muscles and mandibular kinematics in eleven young subjects were recorded. The masticatory parameters were derived from the recorded data for the entire mastication process, for the first bite, and in the early, middle, and late stages of mastication. After calculating values relative to the mean value for each subject, nine parameters representing each group were chosen through a cluster analysis. Three principal components were extracted, each of them related to the masticatory time and cycle, minimum jaw opening at the early stage of mastication, and masticatory force. The principal component scores for each food were different, except for one combination in which the physical properties under large and extra-large deformations were similar, despite different breaking properties or small deformation properties. The masticatory parameters did not correlate with the physical properties of food measured for small deformation.     

Characterization of food physical properties by the mastication parameters measured by electromyography of the jaw-closing muscles and mandibular kinematics in young adults

The relationship between the physical properties of solid food and the masticatory parameters is clarified. Eight solid foods of varying physical properties were chosen. Electromyography of the jaw-closing muscles and mandibular kinematics in eleven young subjects were recorded. The masticatory parameters were derived from the recorded data for the entire mastication process, for the first bite, and in the early, middle, and late stages of mastication. After calculating values relative to the mean value for each subject, nine parameters representing each group were chosen through a cluster analysis. Three principal components were extracted, each of them related to the masticatory time and cycle, minimum jaw opening at the early stage of mastication, and masticatory force. The principal component scores for each food were different, except for one combination in which the physical properties under large and extra-large deformations were similar, despite different breaking properties or small deformation properties. The masticatory parameters did not correlate with the physical properties of food measured for small deformation.     

Comparing apples and oranges—the influence of food mechanical properties on ingestive bite sizes in lemurs

Previously we found that Maximum Ingested Bite Size (V_b)—the largest piece of food that an animal will ingest whole without biting first—scales isometrically with body size in 17 species of strepsirrhines at the Duke Lemur Center (DLC). However, because this earlier study focused on only three food types (two with similar mechanical properties), it did not yield results that were easily applied to describing the broad diets of these taxa. Expressing V_b in terms of food mechanical properties allows us to compare data across food types, including foods of wild lemurs, to better understand dietary adaptations in lemurs. To this end, we quantified V_b in five species of lemurs at the DLC representing large and small frugivores and folivores using ten types of food that vary widely in stiffness and toughness to determine how these properties relate to bite sizes. We found that although most species take smaller bites of stiffer foods, this negative relationship was not statistically significant across the whole sample. However, there is a significant relationship between bite size and toughness. All three of the more frugivorous taxa in our sample take significantly smaller bites of tougher foods. However, the two more folivorous lemurs do not. They take small bites for all foods. This suggests that the species most adapted to the consumption of tough foods do not modulate their ingestive sizes to accommodate larger pieces of weak foods. Am J Phys Anthropol 157:513–518, 2015. © 2015 Wiley Periodicals, Inc.     

Ecological consequences of scaling of chew cycle duration and daily feeding time in Primates

Feeding systems and behaviors must evolve to satisfy the metabolic needs of organisms. This includes modifications to feeding systems as body size and metabolic needs change. Using our own data and data from the literature, we examine how size-related changes in metabolic needs are met by size-related changes in daily feeding time, chew cycle duration, volume of food processed per chew, and daily food volume intake in primates. Increases in chew cycle duration with body mass in haplorhine primates are described by a simple power function (cycle time α body mass^0.181). Daily feeding time increases with body mass when analyzed using raw data from the “tips” of the primate phylogenetic tree, but not when using phylogenetically independent contrasts. Whether or not daily feeding time remains constant or increases with body mass, isometry of ingested bite size and the slow rate of increase in chew cycle time with body size combine to allow daily ingested food volume to scale faster than predicted by metabolic rate. This positive allometry of daily ingested food volume may compensate for negative allometry of nutrient concentration in primate foods. Food material properties such as toughness and hardness have little impact on scaling of chew cycle durations, sequence durations, or numbers of chews in a sequence. Size-related changes in food processing abilities appear to accommodate size-related changes in food material properties, and primates may alter ingested bite sizes in order to minimize the impacts of food material properties on temporal variables such as chew cycle duration and chew sequence duration.     

Food choice by older people: the use of semi-structured interviews with open and closed questions

Objective: To evaluate difficulty chewing, consequent food choice and impacts using both open and closed questions within a semi‐structured interview format. Design: A cross‐sectional study using a semi‐structured interview (SSI) with open and closed questions Setting: Independently living people in South‐West London interviewed in their own homes Subjects: A group of 54, edentate people (mean age 82, R= 60‐93 years) were studied. Results: Most subjects (69%) expressed difficulty eating at least one type of food, half were unwilling to eat the foods they found difficult, others were conscious of cooking longer or cutting smaller in order to manage these foods, although no one accepted that they overcooked food. There were dramatic differences in the number of subjects expressing difficulty to chew various foods when responding to open and closed questions. Roast beef proved a good discriminator in this group of predominantly English subjects. The importance of the questioning process was also shown by the discrepancy of responses between variously prepared apples and the inability of any subjects to bite an unpeeled apple. Conclusions: For sensitive appraisal of food choice it is obviously essential to assess relevant foods, for the culture of the group being studied. Open questions provide a way of exploring which are the appropriate foods and food preparation as criteria to assess perceived chewing ability and treatment benefit. The semi‐structured interview method is particularly valuable for the study of older people. Closed questions provide different information which is also necessary to secure recall by older people.     

Bite force and occlusal stress production in hominin evolution

Maximum bite force affects craniofacial morphology and an organism's ability to break down foods with different material properties. Humans are generally believed to produce low bite forces and spend less time chewing compared with other apes because advances in mechanical and thermal food processing techniques alter food material properties in such a way as to reduce overall masticatory effort. However, when hominins began regularly consuming mechanically processed or cooked diets is not known. Here, we apply a model for estimating maximum bite forces and stresses at the second molar in modern human, nonhuman primate, and hominin skulls that incorporates skeletal data along with species‐specific estimates of jaw muscle architecture. The model, which reliably estimates bite forces, shows a significant relationship between second molar bite force and second molar area across species but does not confirm our hypothesis of isometry. Specimens in the genus Homo fall below the regression line describing the relationship between bite force and molar area for nonhuman anthropoids and australopiths. These results suggest that Homo species generate maximum bite forces below those predicted based on scaling among australopiths and nonhuman primates. Because this decline occurred before evidence for cooking, we hypothesize that selection for lower bite force production was likely made possible by an increased reliance on nonthermal food processing. However, given substantial variability among in vivo bite force magnitudes measured in humans, environmental effects, especially variations in food mechanical properties, may also be a factor. The results also suggest that australopiths had ape‐like bite force capabilities. Am J Phys Anthropol 151:544–557, 2013. © 2013 Wiley Periodicals, Inc.     

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.     

Active stress during compression testing of various foods measured using a multiple-point sheet sensor

Using a multiple-point sheet sensor (MSS), load and contact area were directly measured for compression of four different foods. The MSS provided temporal and spatial changes in stress applied on the sample surface during the testing. The sum of load value detected by the MSS corresponded to the load measured by a universal testing machine during the compression. The contact area between a flat probe and food surface varied with the variety of foods even though under a small strain, and increased as compression strain increased. The active stress, that is, the load divided by the contact area, was different from conventional stress, that is, the load divided by the initial cross-sectional area. The value of active stress provided a better explanation of textural characteristics of food, because texture is often sensed under a large deformation and mixed assessment of mechanical and geometrical properties.     

Temporalis and masseter muscle function during incision in macaques and humans

Most previously published electromyographic (EMG) studies have indicated that the temporalis muscles in humans become almost electrically quiet during incisai biting. These data have led various workers to conclude that these muscles may contribute little to the incisai bite force. The feeding behavior and comparative anatomy of the incisors and temporalis muscles of certain catarrhine primates, however, suggest that the temporalis muscle is an important and powerful contributor to the bite force during incision. One purpose of this study is to analyze the EMG activity of the masseter and temporalis muscles in both humans and macaques with the intention of focusing on the conflict between published EMG data on humans and inferences of muscle function based on the comparative anatomy and behavior of catarrhine primates. The EMG data collected from humans in the present study indicate that, in five of seven subjects, the masseter,anterior temporalis, and posterior temporalis muscles are very active during apple incision (i.e., relative to EMG activity levels during apple and almond mastication). In the other two human subjects the EMG levels of these muscles are lower during incision than during mastication, but in no instance are these muscles ever close to becoming electrically quiet. The EMG data on macaques indicate that, in all six subjects, the masseter, anterior temporalis, and posterior temporalis muscles are very active during incision. These data are in general agreement with inferences on muscle function that have been drawn from the comparative anatomy and behavior of primates, but they do not agree with previous experimental data. The reason for this disagreement is probably due to differences in the experimental procedure. In previous studies subjects simply bit isometrically on their incisors and the resulting EMG pattern was compared to the pattern associated with powerful clenching in centric occlusion. In the present study the subjects incised into actual food objects, and the resulting EMG pattern was compared to the pattern associated with mastication of various foods. It is not surprising that these two procedures result in markedly different EMG patterns, which in turn result in markedly different interpretations of jaw-muscle function. In an attempt to explain the evolution of the postorbital septum in anthropoids, it has been suggested that the anterior temporalis is more active than the masseter during incision (Cachel, 1979). The human and macaque EMG data do not support this hypothesis; during incision, the two muscles show no consistent differences in humans and the masseter appears to be in fact more active than the anterior temporalis in macaques.     

The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements.

Many studies have examined the proportion of time that primates devote to feeding on various types of food, but relatively little is known about the intake rates associated with each food. However, the nutritional consequences of foraging can only be interpreted by comparing nutrient intakes with estimated nutrient requirements. The energy available to primates from ingested foods will depend both on the composition of the food and the extent to which various constituents, including fibre fractions, are digested. Both human and non-human primates have relatively low requirements for protein as a consequence of slow growth rates, small milk yields and relatively dilute milk. Because the nutrient demands of growth and reproduction are spread out over time, it appears that primates do not need to seek out foods of particularly high nutrient density, except perhaps during weaning. Although food selection in some species of primates appears to be correlated with the protein concentration of foods, it is unlikely that high dietary protein levels are required, at least when foods of balanced amino acid composition (such as leaves) are included in the diet.     

Does microbiological testing of foods and the food environment have a role in the control of foodborne disease in England and Wales?

This review looks at the contribution of microbiological sampling to the safety of retail foods in England and Wales. It compares sampling methods available and assesses the value of testing as part of outbreaks of foodborne disease, as part of routine management by local authorities, as part of work done or commissioned by the food industry, and as part of research. It confirms that microbiological testing has a role during outbreaks as it makes a significant contribution to help identify foods and other areas of greatest risk for future study. The review suggests that routine testing by local authorities is often of limited use and could be improved by more targeted surveillance. Testing could be better used to validate primary control methods, such as Hazard Analysis and Critical Control Point (HACCP) system. Any public health benefit from testing in the food industry is often restricted by client confidentiality. Microbial research on foods is important as it can lead to significant improvements in safety. Current microbiological methods are slow and, in future, rapid molecular methods may make an even bigger contribution to the control of foodborne disease.