Peter W. Lucas

Ecological importance of trichromatic vision to primates

Trichromatic colour vision, characterized by three retinal photopigments tuned to peak wavelengths of ∼430 nm, ∼535 nm and ∼562 nm (refs 1, 2), has evolved convergently in catarrhine primates and one genus of New World monkey, the howlers (genus Alouatta). This uniform capacity to discriminate red–green colours, which is not found in other mammals, has been proposed as advantageous for the long-range detection of either ripe fruits or young leaves (which frequently flush red in the tropics) against a background of mature foliage. Here we show that four trichromatic primate species in Kibale Forest, Uganda, eat leaves that are colour discriminated only by red–greenness, a colour axis correlated with high protein levels and low toughness. Despite their divergent digestive systems, these primates have no significant interspecific differences in leaf colour selection. In contrast, eaten fruits were generally discriminated from mature leaves on both red–green and yellow–blue channels and also by their luminance, with a significant difference between chimpanzees and monkeys in fruit colour choice. Our results implicate leaf consumption, a critical food resource when fruit is scarce, as having unique value in maintaining trichromacy in catarrhines.

Global patterns of leaf mechanical properties

Leaf mechanical properties strongly influence leaf lifespan, plant-herbivore interactions, litter decomposition and nutrient cycling, but global patterns in their interspecific variation and underlying mechanisms remain poorly understood. We synthesize data across the three major measurement methods, permitting the first global analyses of leaf mechanics and associated traits, for 2819 species from 90 sites worldwide. Key measures of leaf mechanical resistance varied c. 500-800-fold among species. Contrary to a long-standing hypothesis, tropical leaves were not mechanically more resistant than temperate leaves. Leaf mechanical resistance was modestly related to rainfall and local light environment. By partitioning leaf mechanical resistance into three different components we discovered that toughness per density contributed a surprisingly large fraction to variation in mechanical resistance, larger than the fractions contributed by lamina thickness and tissue density. Higher toughness per density was associated with long leaf lifespan especially in forest understory. Seldom appreciated in the past, toughness per density is a key factor in leaf mechanical resistance, which itself influences plant-animal interactions and ecosystem functions across the globe.

Food physics and oral physiology

Abstract This paper is a review of mastication and swallowing, prepared for the Food Summit on “Food Texture: Perception and Measurement”, organized by the Wageningen Centre for Food Sciences (WCFS) from 28 November–1 December, 1999. The paper emphasizes models that could link the physical state of food to oral forces acting on it. It deals with the processing of solid foods because (1) theory seems better advanced in this area and (2) the paper by van Vliet (this issue) deals with the area of liquids and semi-solids.

Food Properties that Influence Neuromuscular Activity During Human Mastication

The rate of breakdown of food in mastication depends on the ratio of two mechanical properties of the food-the toughness and modulus of elasticity (Agrawal et al., 1997)-a result which can be predicted by an analysis of the energetics of fracture. The work input to produce food fragmentation is provided by the masticatory muscles, the activity levels of which depend on sensory feedback from the mouth. Here, we test the hypothesis that the activity of a representative of this musculature is modulated by the above combination of food properties. The surface electrical activity (EMG) of the anterior temporalis muscles of ten human subjects was recorded while subjects chewed standardized volumes of 15 food types. The integrated EMG in these muscles was highly significantly related to the square root of the ratio of the above two food properties. Significant correlations were found between this food property index and integrated EMG, both when data for all chews and all subjects were lumped together (r = -0.86; p < 0.0001) and when correlation coefficients between the index and EMG were plotted for each chew made by each subject. Except for two subjects in the first chew, these coefficients reached and maintained highly significant levels throughout the masticatory sequence. Thus, a clear relationship between the electrical activity of a jaw-closing muscle and the mechanical properties of food has been found for the first time.

Methods for analysing the breakdown of food in human mastication

A method is described for measuring the rate at which carrot particles are broken down in chewing. In 10 subjects, this rate declined progressively throughout mastication. This was analysed in terms of two variables: (a) the intra-oral selection of particles for fracture, (b) the size distribution of fractured pieces of those particles. When intra-oral selection was measured by different methods, it depended mainly upon particle size. The selection of small particles might depend on the number of chews taken after the food was placed in the mouth. The size distribution of fractured pieces was obtained from one chew on three different particle sizes. These distributions were partially described by two different equations whose characteristics suggest that carrot particles are subjected to only one breakage per chew and that the number of fragments formed per breakage is small. It is suggested that the cusps present on the post-canines were important in determining this breakage pattern, and that the dependence of selection on particle size was primarily responsible for the decline in the rate of breakdown with increasing numbers of chews.

Mechanisms and causes of wear in tooth enamel: implications for hominin diets

The wear of teeth is a major factor limiting mammalian lifespans in the wild. One method of describing worn surfaces, dental microwear texture analysis, has proved powerful for reconstructing the diets of extinct vertebrates, but has yielded unexpected results in early hominins. In particular, although australopiths exhibit derived craniodental features interpreted as adaptations for eating hard foods, most do not exhibit microwear signals indicative of this diet. However, no experiments have yet demonstrated the fundamental mechanisms and causes of this wear. Here, we report nanowear experiments where individual dust particles, phytoliths and enamel chips were slid across a flat enamel surface. Microwear features produced were influenced strongly by interacting mechanical properties and particle geometry. Quartz dust was a rigid abrasive, capable of fracturing and removing enamel pieces. By contrast, phytoliths and enamel chips deformed during sliding, forming U-shaped grooves or flat troughs in enamel, without tissue loss. Other plant tissues seem too soft to mark enamel, acting as particle transporters. We conclude that dust has overwhelming importance as a wear agent and that dietary signals preserved in dental microwear are indirect. Nanowear studies should resolve controversies over adaptive trends in mammals like enamel thickening or hypsodonty that delay functional dental loss.

Swallow thresholds in human mastication.

Brazil-nut particles were broken down and classified by sieves into four classes of particle size. Samples of these classes were suspended in plain yoghurt in varying concentrations and presented to nine humans for chewing. Both the number of chews made before swallowing and the time needed to swallow increased significantly with particle size and concentration but the chewing frequency (number of chews/time) decreased. The rate of change of the chewing frequency, averaged over the chewing sequence (chewing frequency/time), was calculated for each food input and termed the swallowing index. This index did not differ significantly for concentrations above 20%, but increased sharply at lower concentrations. These results were interpreted in terms of a model in which food is swallowed only when particles are both small enough and sufficiently lubricated. For our food mixture, the lubrication threshold was satisfied by a 20% concentration and the particle-size threshold was 1.4 mm. Chews made with concentrations lower than this and containing smaller particle sizes were few in number and slow, reflecting the need to detect particle size with the oral mucosa.

Remarkable resilience of teeth

Tooth enamel is inherently weak, with fracture toughness comparable with glass, yet it is remarkably resilient, surviving millions of functional contacts over a lifetime. We propose a microstructural mechanism of damage resistance, based on observations from ex situ loading of human and sea otter molars (teeth with strikingly similar structural features). Section views of the enamel implicate tufts, hypomineralized crack-like defects at the enamel–dentin junction, as primary fracture sources. We report a stabilization in the evolution of these defects, by “stress shielding” from neighbors, by inhibition of ensuing crack extension from prism interweaving (decussation), and by self-healing. These factors, coupled with the capacity of the tooth configuration to limit the generation of tensile stresses in largely compressive biting, explain how teeth may absorb considerable damage over time without catastrophic failure, an outcome with strong implications concerning the adaptation of animal species to diet.

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.

Chewing It over: Basic Principles of Food Breakdown

In order to meet their metabolic needs, mammals achieve a faster rate of digestion by adding oral processing of solids to the sequence of digestive processes which occur further down the gut. They presumably evolved a mechanical system, rather than increasing the length of their guts, because the cost of mechanical processing is less than the cost of carrying around very large quantities of food. Since increased locomotor activity accompanied, and may have depended on, an increased metabolic rate in comparison to reptiles (Martin, 1980), an increase in inert bulk is not a good solution to the problem.