Variation in carbon isotope values among chimpanzee foods at Ngogo, Kibale National Park and Bwindi Impenetrable National Park, Uganda.

Stable isotope values in primate tissues can be used to reconstruct diet in the absence of direct observation. However, in order to make dietary inferences, one must first establish isotopic variability for potential food sources. In this study we examine stable carbon isotope (δ(13) C) values for chimpanzee (Pan troglodytes) food resources from two Ugandan forests: Ngogo (Kibale National Park), and Bwindi Impenetrable National Park. Mean δ(13) C values for plant samples are equivalent at both sites. Plant δ(13) C values are best explained by a multivariate linear model including plant part (leaves, pith, flowers, and fruit), vertical position within the canopy (canopy vs. ground), and taxon (R(2) = 0.6992). At both sites, leaves had the lowest δ(13) C values followed by pith and fruit. Canopy resources have comparable δ(13) C values at the two sites but ground resources have lower δ(13) C values at Ngogo than Bwindi (-30.7 vs. -28.6‰). Consequently, isotopic differences between ground and canopy resources (4.2 vs. 2.2‰), and among plant parts are more pronounced at Ngogo. These results demonstrate that underlying environmental differences between sites can produce variable δ(13) C signatures among primate food resources. In the absence of observation data or isotope values for local vegetation, caution must be taken when interpreting isotopic differences among geographically or temporally separated populations or species. Am. J. Primatol. 78:1031-1040, 2016. © 2016 Wiley Periodicals, Inc.

Chimpanzee isotopic ecology: a closed canopy C3 template for hominin dietary reconstruction.

The most significant hominin adaptations, including features used to distinguish and/or classify taxa, are critically tied to the dietary environment. Stable isotopic analyses of tooth enamel from hominin fossils have provided intriguing evidence for significant C4/CAM (crassulacean acid metabolism) resource consumption in a number of Plio-Pleistocene hominin taxa. Relating isotopic tooth signatures to specific dietary items or proportions of C3 versus C4/CAM plants, however, remains difficult as there is an ongoing need to document and quantify isotopic variability in modern ecosystems. This study investigates the ecological variables responsible for carbon isotopic discrimination and variability within the C3-dominated dietary niche of a closed canopy East African hominoid, Pan troglodytes, from Ngogo, Kibale National Park, Uganda. δ(13)C values among C3 resources utilized by Ngogo chimpanzees were highly variable, ranging over 13‰. Infrequent foraging on papyrus (the only C4 plant consumed by chimpanzees at the site) further extended this isotopic range. Variation was ultimately most attributable to mode of photosynthesis (C3 versus C4), food type, and elevation, which together accounted for approximately 78% of the total sample variation. Among C3 food types, bulk carbon values ranged from -24.2‰ to -31.1‰ with intra-plant variability up to 12.1‰. Pith and sapling leaves were statistically more (13)C depleted than pulp, seeds, flowers, cambium, roots, leaf buds, and leaves from mature trees. The effect of elevation on carbon variation was highly significant and equivalent to an approximately 1‰ increase in δ(13)C for every 150 m of elevation gain, likely reflecting habitat variability associated with topography. These results indicate significant δ(13)C variation attributable to food type and elevation among C3 resources and provide important data for hominin dietary interpretations based on carbon isotopic analyses.

Diurnal variation in nutrients and chimpanzee foraging behavior.

Primate feeding behavior varies over long (e.g., weekly, seasonally, yearly) and short (e.g., hourly) scales of time due to changes in resource availability and the nutritional composition of foods. While the factors that affect long-term changes in feeding behavior have received considerable attention, few data exist regarding what drives variability in feeding behavior over the course of a single day. To address this problem, we investigated diurnal variation in chimpanzee feeding on the leaves of two species of saplings, Pterygota mildbraedii and Celtis africana, at Ngogo, Kibale National Park, Uganda. Specifically, we related short-term changes in chimpanzee feeding behavior on these leaves to diurnal variation in their nutritional composition. Results showed that chimpanzees fed on the leaves of both saplings more in the evening than they did in the morning. The nutritional quality of leaves also improved over the course of the day. Concentrations of cellulose and lignin were lower and total nonstructural carbohydrates (including sugars and starch) were higher in the evening for P. mildbraedii, and sugars were higher in the evening for C. africana. These data suggest that chimpanzees consume these resources when their quality is highest, and consequently, may track the nutrient composition of their foods over very short periods that span only a few hours. In the future, foods collected for analyses must control for time of sampling to ensure biologically meaningful assays of nutrient composition.

Diurnal variation in glutathione and cysteine redox states in human plasma.

BACKGROUND: Plasma glutathione/glutathione disulfide (GSH/GSSG) and cysteine/cystine (Cys/CySS) couples are oxidized in humans in association with oxidative stress and cardiovascular disease risk. Animal studies show that both pools undergo diurnal variations associated with dietary intake of sulfur amino acids. OBJECTIVE: The objective of this study was to determine whether the redox state of GSH, Cys, GSH/GSSG, or Cys/CySS undergoes diurnal variation in healthy adults. DESIGN: Plasma samples were collected every hour for 24 h from 63 persons aged 18-86 y who were consuming normal food (protein, 0.8 g kg(-1) d(-1); sulfur amino acids, 20 mg kg(-1) d(-1)) at standardized mealtimes. Measurements of Cys, CySS, GSH, and GSSG were used with the Nernst equation to calculate the redox states. RESULTS: Plasma Cys and GSH concentrations varied with the time of day. The highest values for plasma Cys occurred approximately 3 h after meals. Glutathione was maximal 6 h after peak plasma Cys. The calculated redox states of the GSH/GSSG and Cys/CySS couples varied in association with the concentrations of the thiol forms. Maximal reduction and oxidation of the Cys/CySS couple occurred at 2130 and 0630, whereas the respective values for the GSH/GSSG couple occurred at 0330 and 1330. The mean diurnal variation for Cys/CySS redox in persons aged >or=60 y was 1.8-fold that in persons aged <40 y. CONCLUSIONS: Cys/CySS and GSH/GSSG redox states in human plasma undergo diurnal variation with an increased magnitude of variation in Cys/CySS redox state in older persons. This variation could alter sensitivity to oxidative stress over a course of hours.

Docosahexaenoic acid biosynthesis and dietary contingency: Encephalization without aquatic constraint.

Reconstructing evolutionary processes in the distant past is necessarily an inductive endeavor, typically appealing to numerous considerations thought to be relevant to the veracity of a particular conclusion. In this respect, it is essential that the considerations invoked to support hypotheses are in turn well-established truths. It is with these concerns that we sought to examine the nutritional, physiological, and archeological premises underlying the perspective that access to an aquatic diet rich in docosahexaenoic acid (DHA, 22:6n-3) was critical to human brain evolution (Carlson and Kingston [2007]: Am J Hum Biol 19:132-141). In our report investigating links between omega-3 (n-3) fatty acids and hominin encephalization, we concluded that the regular consumption of aquatic resources rich in preformed DHA may not have been essential given a varied diet of wild terrestrial foods (Carlson and Kingston [2007]). This assessment was based primarily on evidence of potential physiological adaptations in modern humans to ensure sufficient availability of DHA during critical periods of brain growth. While modern human physiology provides critical information regarding DHA as a constraint in evolving a large brain, it is also important to consistently contextualize interpretations within a framework of eclectic foraging diets rather than nutritionally limited modern agricultural populations or even modern foragers. We contend that current interpretations of Pleistocene hominin nutritional ecology do not uniquely support a shore-based foraging niche as claimed by Cunnane et al. ([2007]: Am J Hum Biol, 19:578-581). Specific issues raised in response to our article by Cunnane et al. and Joordens et al. ([2007]: Am J Hum Biol, 19:582-584) are addressed here.

Docosahexaenoic acid, the aquatic diet, and hominin encephalization: difficulties in establishing evolutionary links.

Distinctive characteristics of modern humans, including language, tool manufacture and use, culture, and behavioral plasticity, are linked to changes in the organization and size of the brain during hominin evolution. As brain tissue is metabolically and nutritionally costly to develop and maintain, early hominin encephalization has been linked to a release of energetic and nutritional constraints. One such nutrient-based approach has focused on the n-3 long-chained polyunsaturated fatty acid docosahexaenoic acid (DHA), which is a primary constituent of membrane phospholipids within the synaptic networks of the brain essential for optimal cognitive functioning. As biosynthesis of DHA from n-3 dietary precursors (alpha-linolenic acid, LNA) is relatively inefficient, it has been suggested that preformed DHA must have been an integral dietary constituent during evolution of the genus Homo to facilitate the growth and development of an encephalizing brain. Furthermore, preformed DHA has only been identified to an appreciable extent within aquatic resources (marine and freshwater), leading to speculation that hominin encephalization is linked specifically to access and consumption of aquatic resources. The key premise of this perspective is that biosynthesis of DHA from LNA is not only inefficient but also insufficient for the growth and maturation demands of an encephalized brain. However, this assumption is not well-supported, and much evidence instead suggests that consumption of LNA, available in a wider variety of sources within a number of terrestrial ecosystems, is sufficient for normal brain development and maintenance in modern humans and presumably our ancestors.