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.     

Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet

Three categories of dietary adaptation are recognized—faunivory, frugivory, and folivory—according to the distinctive structural and biochemical features of animal matter, fruit, and leaves respectively, and the predominance of only one in the diets of most species. Mammals subsisting mainly on animal matter have a simple stomach and colon and a long small intestine, whereas folivorous species have a complex stomach and/or an enlarged caecum and colon; mammals eating mostly fruit have an intermediate morphology, according to the nature of the fruit and their tendency to supplement this diet with either animal matter or leaves. The frugivorous group are mostly primates: 50 of the 78 mammalian species, and 117 of the 180 individuals included in this analysis are primates. Coefficients of gut differentiation, the ratio of stomach and large intestine to small intestine (by area, weight, and volume), are low in faunivores and high in folivores; the continuous spread of coefficients reflects the different degrees of adaptation to these two dietary extremes. Interspecific comparisons are developed by allowing for allometric factors. In faunivores, in which fermentation is minimal, the volume of stomach and large intestine is related to actual body size, whereas these chambers are more voluminous in larger frugivores and mid-gut fermenting folivores; fore-gut fermenters show a marked decrease in capacity with increasing body size. Surface areas for absorption are related to metabolic body size, directly so in frugivores; area for absorption is relatively less in larger faunivores and more in larger folivores, especially those with large stomachs. Indices of gut specialization are derived from these regressions by nonlinear transformation, with references to the main functional features of capacity for fermentation and surface area for absorption. These are directly comparable with the dietary index, derived from quantitative feeding data displayed on a three-dimensional graph, with all species within a crescentic path from 100% faunivory through 557ndash;80% frugivory to 100% folivory, perhaps illustrating, at least for primates, the evolutionary path from primitive insectivorous forms through three major ecological grades.     

Tooth cusp sharpness as a dietary correlate in great apes

Mammalian molars have undergone heavy scrutiny to determine correlates between morphology and diet. Here, the relationship between one aspect of occlusal morphology, tooth cusp radius of curvature (RoC), and two broad dietary categories, folivory and frugivory, is analyzed in apes. The author hypothesizes that there is a relationship between tooth cusp RoC and diet, and that folivores have sharper teeth than frugivores, and further test the correlation between tooth cusp RoC and tooth cusp size. Eight measures of tooth cusp RoC (two RoCs per cusp) were taken from 53 M²s from four species and subspecies of frugivorous apes (Pongo pygmaeus, Pan troglodytes troglodytes, Pan troglodytes schweinfurthii, and Gorilla gorilla gorilla) and two subspecies of folivorous apes (Gorilla beringei beringei, and Gorilla beringei graueri). Phylogenetically corrected ANOVAs were run on the full dataset and several subsets of the full dataset, revealing that, when buccolingual RoCs are taken into account, tooth cusp RoCs can successfully differentiate folivores and frugivores. PCAs revealed that folivores consistently had duller teeth than frugivores. In addition, a weak, statistically significant positive correlation exists between tooth cusp size and tooth cusp RoC. The author hypothesizes differences in tooth cusp RoC are correlated with wear rates, where, per vertical unit of wear, duller cusps will have a longer length of exposed enamel ridge than sharper cusps. More data need to be gathered to determine if the correlation between tooth cusp RoC and tooth cusp size holds true when small primates are considered. Am J Phys Anthropol 153:226–235, 2014. © 2013 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.     

Dental topography and diets of platyrrhine primates

Abstract

More than half a century ago, Percy Butler touted the importance of analyzing teeth to understand their function in an evolutionary context. There have been many advances in the study of dental functional morphology since that time. Here we review the various approaches to characterizing and comparing occlusal form that have been developed, especially dental topographic analysis. We also report on a new study of dental topography of platyrrhine primates (n = 341 individuals representing 16 species) with known differences in both dietary preferences and other food items eaten. Results indicate frugivores, gummivores, folivores, and seed eaters each have a unique combination of slope, relief, angularity, sharpness, and occlusal orientation patch size and count values. Likewise, among frugivores, those that supplement their diets with hard objects, insects, leaves, and seeds, also each have a distinctive suite of topographic features. We conclude that both primary and secondary diet choices select for occlusal form, and that functional morphology more reflects the types of foods and mechanical challenges they pose rather than the frequencies in which they are eaten.     

Molar microwear in extant small-bodied faunivorous mammals: An analysis of feature density and pit frequency

This study quantitatively examined molar microwear in nine species of extant small-bodied faunivorous primates and microchiropterans. Comparative analyses were performed within the food category faunivory, both between hard- and soft-object feeding faunivores and between primarily insectivorous and carnivorous taxa. Additionally, microwear in faunivores was compared to that reported in the literature for frugivorous and folivorous primates. The results indicated that although insectivores and carnivores could not be distinguished by microwear analyses, hard-object faunivores (i. e., those that primarily consume beetles or actively comminute bone) can be readily distinguished from soft-object faunivores (i. e., moth, caterpillar, or vertebrate flesh specialists). The hard-object faunivores consistently exhibited greater pit frequencies (in excess of 40%). Furthermore, comparisons of these microwear data on faunivorous mammals to previous work on frugivorous and folivorous primates (Teaford, 1988, pers. comm.; Teaford and Runestad, 1992, pers. comm.; Teaford and Walker: American Journal of Physical Anthropology 64:191–200, 1984) permitted three observations to be made. 1) Faunivores tend to have higher mean feature densities than either frugivores or folivores, although these differences are not consistently statistically distinct. 2) Faunifores and frugivores that feed on hard-objects have comparable mean pit frequencies. 3) Although it is impossible to distinguish faunivores and folivores on the basis of metric analysis of gross molar morphology, this distinction can be made on microwear criteria. Both hard- and soft-object faunivores exhibit much higher mean pit frequencies than primarily folivorous species. © 1993 Wiley-Liss, Inc.     

Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques

Primate life histories are strongly influenced by both body and brain mass and are mediated by food availability and perhaps dietary adaptations. It has been suggested that folivorous primates mature and reproduce more slowly than frugivores due to lower basal metabolic rates as well as to greater degrees of arboreality, which can lower mortality and thus fecundity. However, the opposite has also been proposed: faster life histories in folivores due to a diet of abundant, protein-rich leaves. We compared two primate taxa often found in sympatry: Asian colobines (folivores, 11 species) and Asian macaques (frugivores, 12 species). We first described new data for a little-known colobine (Phayre's leaf monkeys, Trachypithecus phayrei crepusculus) from Phu Khieo Wildlife Sanctuary, Thailand. We then compared gestation periods, ages at first birth, and interbirth intervals in colobines and macaques. We predicted that heavier species would have slower life histories, provisioned populations would have faster life histories, and folivores would have slower life histories than frugivores. We calculated general regression models using log body mass, nutritional regime, and taxon as predictor variables. Body mass and nutritional regime had the predicted effects for all three traits. We found taxonomic differences only for gestation, which was significantly longer in colobines, supporting the idea of slower fetal growth (lower maternal energy) compared to macaques and/or advanced dental or gut development. Ages at first birth and interbirth intervals were similar between taxa, perhaps due to additional factors (e.g., allomothering, dispersal). Our results emphasize the need for additional data from wild populations and for establishing whether growth data for provisioned animals (folivores in particular) are representative of wild ones.     

Teeth, brains, and primate life histories

This paper explores the correlates of variation in dental development across the order Primates. We are particularly interested in how 1) dental precocity (percentage of total postcanine primary and secondary teeth that have erupted at selected absolute ages and life cycle stages) and 2) dental endowment at weaning (percentage of adult postcanine occlusal area that is present at weaning) are related to variation in body or brain size and diet in primates. We ask whether folivores have more accelerated dental schedules than do like-sized frugivores, and if so, to what extent this is part and parcel of a general pattern of acceleration of life histories in more folivorous taxa. What is the adaptive significance of variation in dental eruption schedules across the order Primates? We show that folivorous primate species tend to exhibit more rapid dental development (on an absolute scale) than comparably sized frugivores, and their dental development tends to be more advanced at weaning. Our data affirm an important role for brain (rather than body) size as a predictor of both absolute and relative dental development. Tests of alternative dietary hypotheses offer the strongest support for the foraging independence and food processing hypotheses.     

Dietary selection of L'Hoest monkeys in Kalinzu forest reserve, southwestern Uganda

Reports on patterns of dietary selection of forest guenons tend to be general and often classify Cercopithecus l’hoesti as a frugivores–folivores species just like the other guenons, and to date there has been no systematic investigation into the inventory of the species’ food items in the remaining forest fragments to guide major conservation and management decisions. Here we report on the L’Hoest monkeys’ main food species and how the selection of these foods varies among different age groups of the troop in Kalinzu Forest, Uganda for a period of 12 months. Behavioural observations were determined using scan samples [Behaviour, 49 (1974) 227]. Two hypotheses were evaluated in this study. Results indicate that individuals of different age groups have the ability to select a variety of both plant and invertebrate food items in the vicinity to supplement their diets. There was no significant difference in dietary selection between different age groups of L’Hoest monkey for a particular food type (ANOVA: Column analysis, F_3,84 = 1.541337, P = 0.209827). However, significant difference was realized in dietary selection of the different food types by a particular age group (ANOVA: F_22,46 = 40.86429, P = 3.69 × 10^?23). Selective predation pressure against the infants and juveniles by Stephanoaetus coronatus was believed to be one of the likely reasons why infants and juveniles least exposed themselves in the trees feeding on fruits of Musanga leo‐errerae and Ficus spp. Invertebrate feeding was found to constitute high percentage (47.2%) of the species diet and plant materials comprised (52.8%) than previously reported in other study sites. These data provide potentially useful insight on the feeding ecology of the little studied C. l’hoesti and can provide baseline information on conservation of its food items in the remaining forests.     

Daily lettuce supplements promote foraging behavior and modify the gut microbiota in captive frugivores

For captive primates, greater provisioning of leafy greens or foliage can promote natural foraging behavior while boosting fiber intake. Recalcitrant fiber, although minimally available to endogenous metabolism, is readily fermented into nutrients by gut microbes. Whereas most primates in captivity consume fiber-limited diets and harbor imbalanced gut microbiota compared to their wild conspecifics, the importance of fiber provisioning to primate gut microbiota has predominately been studied in folivores. We, therefore, determined if commercial lettuce could be used to encourage foraging behavior and modify the gut microbiota of captive frugivores. We provisioned ruffed lemurs (Varecia rubra and V. variegata) with romaine lettuce, on top of the standard dietary fare, for 10 consecutive days. Before and across the period of lettuce supplementation, we collected observational data of animal feeding and fecal samples for microbiome analysis, determined via amplicon sequencing. The ruffed lemurs and their gut microbes responded to lettuce provisioning. In particular, younger animals readily ate lettuce and showed no decline in consumption across study days. When controlling for the effects of host species and social-group membership, lettuce consumption shifted the composition of the gut microbiome away from each lemur's own baseline, an effect that became stronger as the study progressed. In the final study days, Ruminococcaceae UCG-008 and Akkermansia, microbes typically and respectively associated with fiber metabolism and host health, were significantly enriched in the consortia of lettuce-provisioned subjects. Ultimately, the routine offering of lettuce, leafy greens, or foliage to captive frugivores may benefit animal wellbeing.     

Species co‐occurrence patterns and dietary resource competition in primates

Diamond (Assembly of species communities. In: Cody ML, Diamond JM, editors. Ecology and evolution of communities. Cambridge: Belknap. p 342–444 ( 1975 )) argued that interspecific competition between species occupying similar niches results in a nonrandom pattern of species distributions. In particular, some species pairs may never be found in the same community due to competitive exclusion. Rigorous analytical methods have been developed to investigate the possible role that interspecific competition has on the evolution of communities. Many studies that have implemented these methods have shown support for Diamond's assembly rules, yet there are numerous exceptions. We build on this previous research by examining the co‐occurrence patterns of primate species in 109 communities from across the world. We used EcoSim to calculate a checkerboard (C) score for each region. The C score provides a measure of the proportion of species pairs that do not co‐occur in a set of communities. High C scores indicate that species are nonrandomly distributed throughout a region, and interspecific competition may be driving patterns of competitive exclusion. We conducted two sets of analyses. One included all primate species per region, and the second analysis assigned each species to one of four dietary guilds: frugivores, folivores, insectivores, and frugivore‐insectivores. Using all species per region, we found significantly high C scores in 9 of 10 regions examined. For frugivores, we found significantly high‐C scores in more than 50% of regions. In contrast, only 23% of regions exhibited significantly high‐C scores for folivores. Our results suggest that communities are nonrandomly structured and may be the result of greater levels of interspecific competition between frugivores compared to folivores. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Primates, brains and ecology

The paper examines systematic relationships among primates between brain size (relative to body size) and differences in ecology and social system. Marked differences in relative brain size exist between families. These are correlated with inter-family differences in body size and home range size. Variation in comparative brain size within families is related to diet (folivores have comparatively smaller brains than frugivores), home range size and possibly also to breeding system. The adaptive significance of these relationships is discussed.     

Coping with low-quality diets: a first account of the feeding ecology of the southern gentle lemur, <Emphasis Type="Italic">Hapalemur meridionalis</Emphasis>, in the Mandena littoral forest,southeast Madagascar

Malagasy primates of the genus Hapalemur are exceptional in their exhibition of specialisations allowing for a folivorous diet despite their small body size. Members of this group are well known for their preference for specific parts of woody bamboo, the primary food resource throughout much of their range. The southern gentle lemur (H. meridionalis), however, inhabits littoral forests that contain little or no woody bamboo. Similar to its closely related congener, the Alaotran gentle lemur (H. alaotrensis), the question is raised as to how these lemurs subsist in this ecological context. The aim of this study was to gain an initial understanding of the ecological niche of the southern gentle lemur in the threatened ecosystem of the littoral forest of southeastern Madagascar. Lemurs were habituated and observed over a 3-month period during the austral winter, allowing for collection of both continuous and instantaneous focal data on their feeding ecology. Preferred food species were identified and collected, and biochemical analyses determined macronutrient and secondary compound values for consumed food items. The diet of the southern gentle lemur was found to be of low nutritional quality, as evaluated through the low protein-to-fibre ratio, especially when compared with other folivores. This lemur is also unique in spending a majority of its time grazing on terrestrial grasses (family Poaceae) during the resource-poor winter months. Our data indicate that Hapalemur spp. possess a behavioural flexibility, and possibly, digestive abilities, higher than previously thought for an animal of its small body size.     

Influence of food,body size,and fragmentation on metabolic rate in a sessile marine invertebrate

Metabolic rates vary among individuals according to food availability and phenotype, most notably body size. Disentangling size from other factors (e.g., age, reproductive status) can be difficult in some groups, but modular organisms may provide an opportunity for manipulating size experimentally. While modular organisms are increasingly used to understand metabolic scaling, the potential of feeding to alter metabolic scaling has not been explored in this group. Here, we perform a series of experiments to examine the drivers of metabolic rate in a modular marine invertebrate, the bryozoan Bugula neritina. We manipulated size and examined metabolic rate in either fed or starved individuals to test for interactions between size manipulation and food availability. Field collected colonies of unknown age showed isometric metabolic scaling, but those colonies in which size was manipulated showed allometric scaling. To further disentangle age effects from size effects, we measured metabolic rate of individuals of known age and again found allometric scaling. Metabolic rate strongly depended on access to food: starvation decreased metabolic rate by 20% and feeding increased metabolic rate by 43%. In comparison to other marine invertebrates, however, the increase in metabolic rate, as well as the duration of the increase (known as specific dynamic action, SDA), were both low. Importantly, neither starvation nor feeding altered the metabolic scaling of our colonies. Overall, we found that field‐collected individuals showed isometric metabolic scaling, whereas metabolic rate of size‐manipulated colonies scaled allometrically with body size. Thus, metabolic scaling is affected by size manipulation but not feeding in this colonial marine invertebrate.     

Ontogenetic body-mass scaling of resting metabolic rate covaries with species-specific metabolic level and body size in spiders and snakes

According to common belief, metabolic rate usually scales with body mass to the 3/4-power, which is considered by some to be a universal law of nature. However, substantial variation in the metabolic scaling exponent (b) exists, much of which can be related to the overall metabolic level (L) of various taxonomic groups of organisms, as predicted by the recently proposed metabolic-level boundaries (MLB) hypothesis. Here the MLB hypothesis was tested using data for intraspecific (ontogenetic) body-mass scaling of resting metabolic rate in spiders and boid snakes. As predicted, in both animal groups b varies mostly between 2/3 and 1, and is significantly negatively related to L. L is, in turn, negatively related to species-specific body mass (M_m: estimated as the mass at the midpoint of a scaling relationship), and as a result, larger species tend to have steeper metabolic scaling slopes (b) than smaller species. After adjusting for the effects of M_m, b and L are still negatively related, though significantly only in the spiders, which exhibit a much wider range of L than the snakes. Therefore, in spiders and snakes the intraspecific scaling of metabolic rate with body mass itself scales with interspecific variation in both metabolic level and body mass.     

Scaling with body mass of mitochondrial respiration from the white muscle of three phylogenetically, morphologically and behaviorally disparate teleost fishes

White muscle (WM) fibers in many fishes often increase in size from <50 μm in juveniles to >250 μm in adults. This leads to increases in intracellular diffusion distances that may impact the scaling with body mass of muscle metabolism. We have previously found similar negative scaling of aerobic capacity (mitochondrial volume density, V _mt) and the rate of an aerobic process (post-contractile phosphocreatine recovery) in fish WM. In the present study, we examined the scaling with body mass of oxygen consumption rates of isolated mitochondria (VO_2mt) from WM in three species from different families that vary in morphology and behavior: an active, pelagic species (bluefish, Pomatomus saltatrix), a relatively inactive demersal species (black sea bass, Centropristis striata), and a sedentary, benthic species (southern flounder, Paralichthys lethostigma). In contrast to our prior studies, the measurement of respiration in isolated mitochondria is not influenced by the diffusion of oxygen or metabolites. V _mt was measured in WM and in high-density isolates used for VO_2mt measurements. WM V _mt was significantly higher in the bluefish than in the other two species and VO_2mt was independent of body mass when expressed per milligram protein or per milliliter mitochondria. The size-independence of VO_2mt indicates that differences in WM aerobic function result from variation in V _mt and not to changes in VO_2mt. This is consistent with our prior work that indicated that while diffusion constraints influence mitochondrial distribution, the negative scaling of aerobic processes like post-contractile PCr recovery can largely be attributed to the body size dependence of V _mt.     

Shape shifting predicts ontogenetic changes in metabolic scaling in diverse aquatic invertebrates

Metabolism fuels all biological activities, and thus understanding its variation is fundamentally important. Much of this variation is related to body size, which is commonly believed to follow a 3/4-power scaling law. However, during ontogeny, many kinds of animals and plants show marked shifts in metabolic scaling that deviate from 3/4-power scaling predicted by general models. Here, we show that in diverse aquatic invertebrates, ontogenetic shifts in the scaling of routine metabolic rate from near isometry (b_R = scaling exponent approx. 1) to negative allometry (b_R < 1), or the reverse, are associated with significant changes in body shape (indexed by b_L = the scaling exponent of the relationship between body mass and body length). The observed inverse correlations between b_R and b_L are predicted by metabolic scaling theory that emphasizes resource/waste fluxes across external body surfaces, but contradict theory that emphasizes resource transport through internal networks. Geometric estimates of the scaling of surface area (SA) with body mass (b_A) further show that ontogenetic shifts in b_R and b_A are positively correlated. These results support new metabolic scaling theory based on SA influences that may be applied to ontogenetic shifts in b_R shown by many kinds of animals and plants.     

Allometric scaling in the dentition of primates and prediction of body weight from tooth size in fossils

Tooth size varies exponentially with body weight in primates. Logarithmic transformation of tooth crown area and body weight yields a linear model of slope 0.67 as an isometric (geometric) baseline for study of dental allometry. This model is compared with that predicted by metabolic scaling (slope = 0.75). Tarsius and other insectivores have larger teeth for their body size than generalized primates do, and they are not included in this analysis. Among generalized primates, tooth size is highly correlated with body size. Correlations of upper and lower cheek teeth with body size range from 0.90–0.97, depending on tooth position. Central cheek teeth (P and M) have allometric coefficients ranging from 0.57–0.65, falling well below geometric scaling. Anterior and posterior cheek teeth scale at or above metabolic scaling. Considered individually or as a group, upper cheek teeth scale allometrically with lower coefficients than corresponding lower cheek teeth; the reverse is true for incisors. The sum of crown areas for all upper cheek teeth scales significantly below geometric scaling, while the sum of crown areas for all lower cheek teeth approximates geometric scaling. Tooth size can be used to predict the body weight of generalized fossil primates. This is illustrated for Aegyptopithecus and other Eocene, Oligocene, and Miocene primates. Regressions based on tooth size in generalized primates yield reasonable estimates of body weight, but much remains to be learned about tooth size and body size scaling in more restricted systematic groups and dietary guilds.