Mechanical properties of foods used in experimental studies of primate masticatory function

In vivo studies of jaw-muscle behavior have been integral factors in the development of our current understanding of the primate masticatory apparatus. However, even though it has been shown that food textures and mechanical properties influence jaw-muscle activity during mastication, very little effort has been made to quantify the relationship between the elicited masticatory responses of the subject and the mechanical properties of the foods that are eaten. Recent work on human mastication highlights the importance of two mechanical properties-toughness and elastic modulus (i.e., stiffness)-for food breakdown during mastication. Here we provide data on the toughness and elastic modulus of the majority of foods used in experimental studies of the nonhuman primate masticatory apparatus. Food toughness ranges from approximately 56.97 Jm(-2) (apple pulp) to 4355.45 Jm(-2) (prune pit). The elastic modulus of the experimental foods ranges from 0.07 MPa for gummy bears to 346 MPa for popcorn kernels. These data can help researchers studying primate mastication select among several potential foods with broadly similar mechanical properties. Moreover, they provide a framework for understanding how jaw-muscle activity varies with food mechanical properties in these studies.     

Linking feeding ecology and population abundance: a review of food resource limitation on primates

We review studies that consider how food affects primate population abundance. In order to explain spatial variation in primate abundance, various correlates that parameterize quality and quantity of food in the habitat have been examined. We propose two hypotheses concerning how resource availability and its seasonality determine animal abundance. When the quality of fallback foods (foods eaten during the scarcity of preferred foods) is too low to satisfy nutritional requirement, total annual food quantity should determine population size, but this relationship can be modified by the quality or the quantity of fallback foods. This mechanism has been established for Japanese macaques and sportive lemurs that survive lean seasons by fat storage or extremely low metabolism. Second, when fallback food quality is high enough to satisfy nutritional requirement but quantity is limited, quantity of fallback food should be a limiting factor of animal abundance. This is supported by the correlation between fig density, which is a high-quality fallback food, and gibbon and orangutan abundance. For a direct test of these hypotheses, we need more research that determines both the quality of food that animals require to satisfy their nutritional requirement and the quantity of food production. Leaves are often regarded as superabundant, but this assumption needs careful examination.     

Defining fallback foods and assessing their importance in primate ecology and evolution

Physical anthropologists use the term “fallback foods” to denote resources of relatively poor nutritional quality that become particularly important dietary components during periods when preferred foods are scarce. Fallback foods are becoming increasingly invoked as key selective forces that determine masticatory and digestive anatomy, influence grouping and ranging behavior, and underlie fundamental evolutionary processes such as speciation, extinction, and adaptation. In this article, we provide an overview of the concept of fallback foods by discussing definitions of the term and categorizations of types of fallback foods, and by examining the importance of fallback foods for primate ecology and evolution. We begin by comparing two recently published conceptual frameworks for considering the evolutionary significance of fallback foods and propose a way in which these approaches might be integrated. We then consider a series of questions about the importance of fallback foods for primates, including the extent to which fallback foods should be considered a distinct class of food resources, separate from preferred or commonly eaten foods; the link between life history strategy and fallback foods; if fallback foods always limit primate carrying capacity; and whether particular plant growth forms might play especially important roles as fallback resources for primates. We conclude with a brief consideration of links between fallback foods and primate conservation. Am J Phys Anthropol 140:603–614, 2009. © 2009 Wiley-Liss, Inc.     

Dietary variation and food hardness in sooty mangabeys (Cercocebus atys): Implications for fallback foods and dental adaptation

We present information on food hardness and monthly dietary changes in female sooty mangabeys (Cercocebus atys) in Tai Forest, Ivory Coast to reassess the hypothesis that thick molar enamel is parsimoniously interpreted as a response to consumption of hard foods during fallback periods. We demonstrate that the diet of sooty mangabeys varies seasonally, but that one food—Sacoglottis gabonensis—is the most frequently consumed food every month and year round. This food is the hardest item in the sooty diet. Given that this species has among the thickest enamel within the primate order, a plausible conclusion is that thick enamel in this taxon evolved not in response to seasonally critical function or fallback foods, but rather to the habitual, year round processing of a mechanically protected foodstuff. These data serve as a caution against de rigueur interpretations that reliance on fallback foods during lean periods primarily explains the evolution of thick enamel in primates. Am J Phys Anthropol 154:413–423, 2014. © 2014 Wiley Periodicals, Inc.     

The role of tooth enamel mechanical properties in primate dietary adaptation

Primate teeth adapt to the physical properties of foods in a variety of ways including changes in occlusal morphology, enamel thickness, and overall size. We conducted a comparative study of extant primates to examine whether their teeth also adapt to foods through variation in the mechanical properties of the enamel. Nanoindentation techniques were used to map profiles of elastic modulus and hardness across tooth sections from the enamel-dentin junction to the outer enamel surface in a broad sample of primates including apes, Old World monkeys, New World monkeys, and lemurs. The measured data profiles feature considerable overlap among species, indicating a high degree of commonality in mechanical properties. These results suggest that differences in the load-bearing capacity of primate molar teeth are more a function of morphology-particularly tooth size and enamel thickness-than of underlying mechanical properties.     

Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii

The divergent molar characteristics of Pan troglodytes and Pongo pygmaeus provide an instructive paradigm for examining the adaptive form-function relationship between molar enamel thickness and food hardness. Although both species exhibit a categorical preference for ripe fruit over other food objects, the thick enamel and crenulated occlusal surface of Pongo molar teeth predict a diet that is more resistant to deformation (hard) and fracture (tough) than the diet of Pan. We confirm these predictions with behavioral observations of Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii in the wild and describe the mechanical properties of foods utilized during periods when preferred foods are scarce. Such fallback foods may have exerted a selective pressure on tooth evolution, particularly molar enamel thinness, which is interpreted as a functional adaptation to seasonal folivory and a derived character trait within the hominoid clade. The thick enamel and crenulated occlusal surface of Pongo molars is interpreted as a functional adaptation to the routine consumption of relatively tough and hard foods. We discuss the implications of these interpretations for inferring the diet of hominin species, which possessed varying degrees of thick molar enamel. These data, which are among the first reported for hominoid primates, fill an important empirical void for evaluating the mechanical plausibility of putative hominin food objects.     

Tooth Chipping as a Tool to Reconstruct Diets of Great Apes (Pongo, Gorilla, Pan)

Most methods of dietary reconstruction are limited in their applicability to either extant or extinct taxa. We apply and discuss a method in which dietary information can be reconstructed from chips in the tooth enamel of both living and fossil primates. Such chips can be used to indicate the presence of large hard foods in the diet, and also to provide an estimate of the bite force that was used when the chip was created. Furthermore, the equations derived from this method allow an estimate of maximum bite force to be obtained from a simple measurement of tooth size. We use this method to investigate dietary differences in nonhuman great apes (Pongo, Gorilla, Pan). The high frequency of chips on teeth of Pongo indicate that they frequently use high forces to process hard foods such as seeds and nuts. Gorilla can generate even higher bite forces, but their low incidence of tooth chips suggests that they do so when consuming soft but tough foods. Tooth chips provide a lasting dietary signal that is not easily masked or erased, making them particularly useful for the study of rarely eaten items such as some fallback foods.     

Enamel thickness in Bornean and Sumatran orangutan dentitions

Dental enamel thickness has received considerable attention in ecological models of the adaptive significance of primate morphology. Several authors have theorized that the degree of enamel thickness may reflect selective pressures related to the consumption of fallback foods (dietary items that may require complex processing and/or have low nutritional value) during times of preferred food scarcity. Others have speculated that enamel thickness reflects selection during mastication of foods with particular material properties (i.e., toughness and hardness). Orangutans prefer ripe fruit when available, but show interspecific and sex differences in the consumption of fallback foods (bark, leaves, and figs) and other preferred foods (certain seeds). Bornean orangutans (Pongo pygmaeus) have also been reported to masticate more mechanically demanding foods than Sumatran orangutans (Pongo abelii). To test these ecological models, we assessed two-dimensional enamel thickness in orangutan full dentitions using established histological and virtual quantification methods. No significant differences in average enamel thickness (AET) were found between species. We found significant differences in the components of enamel thickness indices between sexes, with males showing greater enamel-dentine junction lengths and dentine core areas, and thus relatively thinner enamel than females. Comparisons of individuals of known sex and species revealed a dentition-wide trend for Bornean females to show greater AET than Sumatran females. Differences between small samples of males were less evident. These data provide only limited support for ecological explanations of enamel thickness patterns within great ape genera. Future studies of dietary ecology and enamel thickness should consider sex differences more systematically.     

The impact of fallback foods on wild ring-tailed lemur biology: A comparison of intact and anthropogenically disturbed habitats

Fallback foods are often viewed as central in shaping primate morphology, and influencing adaptive shifts in hominin and other primate evolution. Here we argue that fruit of the tamarind tree (Tamarindus indica) qualifies as a fallback food of ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Special Reserve (BMSR), Madagascar. Contrary to predictions that fallback foods may select for dental and masticatory morphologies adapted to processing these foods, consumption of tamarind fruit by these lemurs leaves a distinct pattern of dental pathology among ring-tailed lemurs at BMSR. Specifically, the physical and mechanical properties of tamarind fruit likely result in a high frequency of severe tooth wear, and subsequent antemortem tooth loss, in this lemur population. This pattern of dental pathology is amplified among lemurs living in disturbed areas at Beza Mahafaly, resulting from a disproportionate emphasis on challenging tamarind fruit, due to few other fruits being available. This is in part caused by a reduction in ground cover and other plants due to livestock grazing. As such, tamarind trees remain one of the few food resources in many areas. Dental pathologies are also associated with the use of a nonendemic leaf resource Argemone mexicana, an important food during the latter part of the dry season when overall food availability is reduced. Such dental pathologies at Beza Mahafaly, resulting from the use or overemphasis of fallback foods for which they are not biologically adapted, indicate that anthropogenic factors must be considered when examining fallback foods. Am J Phys Anthropol 140:671–686, 2009. © 2009 Wiley-Liss, Inc.     

The mechanics of the first bite

An analysis of the action of the incisor teeth in humans is presented in terms of the fracture of food particles. It is predicted that the resistance of foods with an essentially linear elastic response to an initial bite by the incisors will depend on the square root of the product of two food properties, Young's modulus and toughness. This quantity should be approximately equal to the product of the stress at cracking during a bite, and the square root of the length of a notch or indentation from which that crack initiates. As a test of the theory, the relationship between in vivo stresses and the depth of incisal penetration, measured during bites on seven 'snack' foods by 10 subjects, and food properties established from mechanical testing, was investigated. Theory and experiment were found to be in excellent agreement. A dimensionless index of the efficiency of incision is suggested, relating fracture performance by subjects to values from a testing machine. This appears to have a high level of inter-subject discrimination with efficiencies varying about threefold. The method appears to have potential applications in dentistry, food science and studies of human and primate evolution.     

Graminivory and Fallback Foods: Annual Diet Profile of Geladas (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>) Living in the Simien Mountains National Park,Ethiopia

All primates show some dietary flexibility, particularly during food shortages. Foods consumed during times of scarcity (i.e., fallback foods) strongly influence the ecology and evolution of a species. Geladas (Theropithecus gelada) eat primarily graminoid leaves (i.e., grasses and sedges), but also consume other diet items (e.g., underground storage organs), especially in the dry season. We investigated the feeding ecology of wild geladas in the Sankaber region of the Simien Mountains National Park, Ethiopia across 12 mo. We asked how the gelada diet in this region, which is disturbed by livestock and agriculture, correlated with food availability and whether underground foods are fallback foods. We quantified the monthly diets of adults from eight reproductive units using instantaneous scan sampling, and seasonal aboveground and underground food availability using point-intercept transects and soil core sampling. Geladas primarily consumed graminoid leaves year-round (76.3% of the annual diet, 36.2–93.2% of the monthly diet) but spent considerable time consuming underground foods in the dry season (14.0% of the annual diet, 11.1–49.7% of the diet across dry season months). Graminoid consumption increased with graminoid availability, and underground food consumption decreased with graminoid availability. Underground food availability did not vary significantly between the dry and wet season sampling months, supporting the hypothesis that underground foods are fallback foods for geladas. We then compiled data from gelada feeding studies and found that underground foods are an important dry season diet item across study sites, but geladas rely more heavily on underground foods in habitats more heavily influenced by humans. Understanding the range and effects of primate dietary flexibility in human-modified habitats will contribute to a better understanding of how changing environments shape primate ecology and evolution.     

Summary to the symposium issue: Primate fallback strategies as adaptive phenotypic plasticity—Scale,pattern, and process

In this discussion, I evaluate our understanding of fallback foods in primate and hominin ecology and evolution with reference to the challenges of nomenclature, scale, and of linking individual responses to food availability and properties (process) to species traits (pattern). I use these challenges to form the framework of my discussion and ultimately conclude that we situate the discussion of primate fallback strategy into a broader, “synthetic” framework of animal form and the evolutionary significance of phenotypic plasticity. Am J Phys Anthropol 140:759–766, 2009. © 2009 Wiley-Liss, Inc.     

Fallback foraging as a way of life: Using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation

The genus Cebus is one of the best extant models for examining the role of fallback foods in primate evolution. Cebus includes the tufted capuchins, which exhibit skeletal features for the exploitation of hard and tough foods. Paradoxically, these seemingly “specialized” taxa belong to the most ubiquitous group of closely related primates in South America, thriving in a range of different habitats. This appears to be a consequence of their ability to exploit obdurate fallback foods. Here we compare the toughness of foods exploited by two tufted capuchin species at two ecologically distinct sites; C. apella in a tropical rainforest, and C. libidinosus in a cerrado forest. We include dietary data for one untufted species (C. olivaceus) to assess the degree of difference between the tufted species. These data, along with information on skeletal morphology, are used to address whether or not a fallback foraging species exhibits a given suite of morphological and behavioral attributes, regardless of habitat. Both tufted species ingest and masticate a number of exceedingly tough plant tissues that appear to be used as fallback resources, however, C. libidinosus has the toughest diet both in terms of median and maximal values. Morphologically, C. libidinosus is intermediate in absolute symphyseal and mandibular measurements, and in measures of postcranial robusticity, but exhibits a higher intermembral index than C. apella. We propose that this incongruence between dietary toughness and skeletal morphology is the consequence of C. libidinosus' use of tools while on the ground for the exploitation of fallback foods. Am J Phys Anthropol 140:687–699, 2009. © 2009 Wiley-Liss, Inc.     

Interpreting food processing through dietary mechanical properties: a Lemur catta case study

Knowledge of dietary mechanical properties can be informative about physical consequences to consumers during ingestion and mastication. In this article, we examine how Tamarindus indica fruits can affect dental morphology in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly special reserve in southwestern Madagascar. Ring-tailed lemurs in tamarind dominated gallery forests exhibit extreme wear and tooth loss on their postcanine dentition that has been related to processing T. indica fruits. We measured and compared mechanical properties of individual food parts in the diet of ring-tailed lemurs in different seasons in 1999-2000, 2008, and 2010. Fracture toughness, hardness, and modulus of foods were measured with a portable mechanical tester. The ripe fruits of T. indica are indeed the toughest and hardest foods ingested by the lemurs. In addition, they are among the largest foods consumed, require high numbers of ingestive bites to process, and are the most frequently eaten by volume. During controlled cutting tests of the ripe fruit shell, multiple runaway side cracks form alongside the cut. Similarly, the lemurs repeatedly bite the ripe shell during feeding and thereby introduce multiple cracks that eventually fragment the shell. Studies of enamel microstructure (e.g., Lucas et al.: BioEssays 30 (2008) 374-385; Campbell et al., 2011) advance the idea that the thin enamel of ring-tailed lemur teeth is susceptible to substantial micro-cracking that rapidly erodes the teeth. We conclude that micro-cracking from repeated loads, in combination with the mechanical and physical properties of the fruit, is primarily responsible for the observed dental damage.     

Evolutionary Consequences of Fallback Foods

Primatologists use the term fallback foods to denote resources of relatively low preference that are used seasonally when preferred foods are unavailable. We examine the assumption that fallback foods play an important role in shaping morphological adaptations, behavior, and socioecology in primates. We discuss operational definitions of preferred and fallback foods and suggest that the evolutionary importance of fallback foods applies more to adaptations for processing than for harvesting foods. Equally, we propose that preferred resources tend to drive adaptations for harvesting foods. We distinguish 2 classes of fallback foods according to their roles in the diet and their evolutionary effects. Staple fallback foods are available year-round, tend to be eaten throughout the year, and seasonally can constitute up to 100% of the diet. Filler fallback foods never constitute 100% of the diet, and may be completely avoided for weeks at a time. We suggest that the availability of the 2 classes of fallback foods have different effects on the socioecology of primate species.     

Craniodental biomechanics and dietary toughness in the genus Cebus

The tufted capuchin (Cebus apella) has been used in a number of comparative studies to represent a primate with craniofacial morphology indicative of hard-object feeding. Researchers have specifically referred to the tufted capuchin as a seed predator. Craniofacial features exhibited by the tufted capuchin, such as thick cortical bone in the mandibular corpus and symphysis, and a broad face associated with large masticatory muscles, permit the production and dissipation of relatively high masticatory forces. These morphologies, however, cannot distinguish between the tufted capuchin's propensity to exert higher forces when opening food with its anterior dentition or with its cheek teeth. It is also unclear whether these are adaptations for biting or chewing foods. This study uses a constrained lever model to compare the masticatory adaptations of C. apella to other cebids and atelids. Results show that the temporalis and masseter muscles in C. apella and C. olivaceus are more anteriorly positioned relative to nine other platyrrhine taxa. This condition, which appears to be ancestral among the Cebinae, increases force production at the incisors and canines while compromising third molar function. Cebus apella, has exaggerated this pattern. Field data on dietary toughness show that both capuchins typically select foods of low toughness, but on occasion, C. apella ingests food items of exceptional toughness. Thus, C. apella appears to maintain these biomechanical relationships by producing particularly high but relatively infrequent bite forces, particularly at the incisors and canines. However, adaptations for anterior dental use do not tightly constrain the diet of Cebus apella. This approach can be used to clarify the dietary adaptations of fossil taxa.     

The importance of fallback foods in primate ecology and evolution

The role of fallback foods in shaping primate ranging, socioecology, and morphology has recently become a topic of particular interest to biological anthropologists. Although the use of fallback resources has been noted in the ecological and primatological literature for a number of decades, few attempts have been made to define fallback foods or to explore the utility of this concept for primate evolutionary biologists and ecologists. As a preface to this special issue of the American Journal of Physical Anthropology devoted to the topic of fallback foods in primate ecology and evolution, we discuss the development and use of the fallback concept and highlight its importance in primatology and paleoanthropology. AmJ Phys Anthropol 140:599–602, 2009. © 2009 Wiley-Liss, Inc.     

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.     

Adaptation to hard-object feeding in sea otters and hominins

The large, bunodont postcanine teeth in living sea otters (Enhydra lutris) have been likened to those of certain fossil hominins, particularly the ’robust’ australopiths (genus Paranthropus). We examine this evolutionary convergence by conducting fracture experiments on extracted molar teeth of sea otters and modern humans (Homo sapiens) to determine how load-bearing capacity relates to tooth morphology and enamel material properties. In situ optical microscopy and x-ray imaging during simulated occlusal loading reveal the nature of the fracture patterns. Explicit fracture relations are used to analyze the data and to extrapolate the results from humans to earlier hominins. It is shown that the molar teeth of sea otters have considerably thinner enamel than those of humans, making sea otter molars more susceptible to certain kinds of fractures. At the same time, the base diameter of sea otter first molars is larger, diminishing the fracture susceptibility in a compensatory manner. We also conduct nanoindentation tests to map out elastic modulus and hardness of sea otter and human molars through a section thickness, and microindentation tests to measure toughness. We find that while sea otter enamel is just as stiff elastically as human enamel, it is a little softer and tougher. The role of these material factors in the capacity of dentition to resist fracture and deformation is considered. From such comparisons, we argue that early hominin species like Paranthropus most likely consumed hard food objects with substantially higher biting forces than those exerted by modern humans.     

Dental microwear texture and anthropoid diets

Dental microwear has long been used as evidence concerning the diets of extinct species. Here, we present a comparative baseline series of dental microwear textures for a sample of 21 anthropoid primate species displaying interspecific and intraspecific dietary variability. Four dental microwear texture variables (complexity, anisotropy, textural fill volume, and heterogeneity) were computed based on scale-sensitive fractal analysis and high-resolution three-dimensional renderings of microwear surfaces collected using a white-light confocal profiler. The purpose of this analysis was to assess the extent to which these variables reflect variation in diet. Significant contrasts between species with diets known to include foods with differing material properties are clearly evident for all four microwear texture variables. In particular, species that consume more tough foods, such as leaves, tended to have high levels of anisotropy and low texture complexity. The converse was true for species including hard and brittle items in their diets either as staples or as fallback foods. These results reaffirm the utility of dental microwear texture analysis as an important tool in making dietary inferences based on fossil primate samples.