Variable digestibility of captive northern greater galagos (Otolemur garnettii) fed experimental "frugivorous" and "invertebrate" diets.

Few studies have addressed the nutritional ecology of galagos. Observations of galagos in the wild reveal that they rely on fruits and invertebrates to varying degrees depending on their availability. We conducted a 6-week comparative dietary analysis of a colony of captive-housed northern greater galagos (Otolemur garnettii), which included five females and six males with known life histories. We compared two experimental diets. The first was fruit dominated and the second was invertebrate dominated. For each diet, we examined dietary intake and apparent dry matter digestibility over the course of 6 weeks. We found significant differences between the apparent digestibility of the diets, with the "invertebrate" diet being more digestible than the "frugivorous" diet. The lower apparent digestibility of the "frugivorous" diet was driven by the higher fiber contents of the fruits provided to the colony. However, variation in apparent digestibility of both diets was found among individual galagos. The experimental design used in this study may provide useful dietary data for the management of captive colonies of galagos and other strepsirrhine primates. This study may also be helpful for understanding the nutritional challenges faced by free-ranging galagos through time and across geographic space.

Dating of a large tool assemblage at the Cooper's Ferry site (Idaho, USA) to ~15,785 cal yr B.P. extends the age of stemmed points in the Americas.

The timing and character of the Pleistocene peopling of the Americas are measured by the discovery of unequivocal artifacts from well-dated contexts. We report the discovery of a well-dated artifact assemblage containing 14 stemmed projectile points from the Cooper's Ferry site in western North America, dating to ~16,000 years ago. These stemmed points are several thousand years older than Clovis fluted points (~13,000 cal yr B.P.) and are ~2300 years older than stemmed points found previously at the site. These points date to the end of Marine Isotope Stage 2 when glaciers had closed off an interior land route into the Americas. This assemblage includes an array of stemmed projectile points that resemble pre-Jomon Late Upper Paleolithic tools from the northwestern Pacific Rim dating to ~20,000 to 19,000 years ago, leading us to hypothesize that some of the first technological traditions in the Americas may have originated in the region.

A 41,500 year-old decorated ivory pendant from Stajnia Cave (Poland).

Evidence of mobiliary art and body augmentation are associated with the cultural innovations introduced by Homo sapiens at the beginning of the Upper Paleolithic. Here, we report the discovery of the oldest known human-modified punctate ornament, a decorated ivory pendant from the Paleolithic layers at Stajnia Cave in Poland. We describe the features of this unique piece, as well as the stratigraphic context and the details of its chronometric dating. The Stajnia Cave plate is a personal 'jewellery' object that was created 41,500 calendar years ago (directly radiocarbon dated). It is the oldest known of its kind in Eurasia and it establishes a new starting date for a tradition directly connected to the spread of modern Homo sapiens in Europe.

Intrataxonomic trends in herbivore enamel δ13C are decoupled from ecosystem woody cover.

Analysis of enamel stable carbon isotopes (δ13Cenamel) of fossil herbivores is an important tool for making inferences about Plio-Pleistocene vegetation structure in Africa and the environmental context of hominin evolution. Many palaeoecological studies implicitly or explicitly assume that individual variation in C3-C4 plant consumption among fossil herbivores directly reflects the abundance of C3 (trees, shrubs) or C4 (low-altitude tropical grasses) vegetation. However, a strong link between δ13Cenamel of herbivores and ecosystem vegetation structure has not been rigorously established. Here we combine δ13Cenamel data from a large dataset (n = 1,643) with multidecadal Landsat estimates of C3 woody cover across 30 African ecosystems to show that there is little relationship between intrataxonomic variation in δ13Cenamel and vegetation structure. This is especially true when removing forested ecosystems (>80% woody cover)-which numerous lines of evidence suggest are rare in the Plio-Pleistocene fossil record of eastern Africa-from our analyses. Our findings stand in contrast with the common assumption that variation in herbivore δ13Cenamel values reflects changes in the relative abundance of C3-C4 vegetation. We conclude that analyses using herbivore δ13Cenamel data to shed light on the environmental context of hominin evolution should look to explicitly community-level approaches for making vegetation inferences.

Dietary trends in herbivores from the Shungura Formation, southwestern Ethiopia.

Diet provides critical information about the ecology and environment of herbivores. Hence, understanding the dietary strategies of fossil herbivores and the associated temporal changes is one aspect of inferring paleoenvironmental conditions. Here, we present carbon isotope data from more than 1,050 fossil teeth that record the dietary patterns of nine herbivore families in the late Pliocene and early Pleistocene (3.6 to 1.05 Ma) from the Shungura Formation, a hominin-bearing site in southwestern Ethiopia. An increasing trend toward C4 herbivory has been observed with attendant reductions in the proportions of browsers and mixed feeders through time. A high proportion of mixed feeders has been observed prior to 2.9 Ma followed by a decrease in the proportion of mixed feeders and an increase in grazers between 2.7 and 1.9 Ma, and a further increase in the proportion of grazers after 1.9 Ma. The collective herbivore fauna shows two major change points in carbon isotope values at ∼2.7 and ∼2.0 Ma. While hominin fossils from the sequence older than 2.7 Ma are attributed to Australopithecus, the shift at ∼2.7 Ma indicating the expansion of C4 grasses on the landscape was concurrent with the first appearance of Paranthropus The link between the increased C4 herbivory and more open landscapes suggests that Australopithecus lived in more wooded landscapes compared to later hominins such as Paranthropus and Homo, and has implications for key morphological and behavioral adaptations in our lineage.

Isotopic evidence for the timing of the dietary shift toward C4 foods in eastern African Paranthropus.

New approaches to the study of early hominin diets have refreshed interest in how and when our diets diverged from those of other African apes. A trend toward significant consumption of C4 foods in hominins after this divergence has emerged as a landmark event in human evolution, with direct evidence provided by stable carbon isotope studies. In this study, we report on detailed carbon isotopic evidence from the hominin fossil record of the Shungura and Usno Formations, Lower Omo Valley, Ethiopia, which elucidates the patterns of C4 dietary utilization in the robust hominin Paranthropus The results show that the most important shift toward C4 foods occurred at ∼2.37 Ma, within the temporal range of the earliest known member of the genus, Paranthropus aethiopicus, and that this shift was not unique to Paranthropus but occurred in all hominins from this fossil sequence. This uptake of C4 foods by hominins occurred during a period marked by an overall trend toward increased C4 grazing by cooccurring mammalian taxa from the same sequence. However, the timing and geographic patterns of hominin diets in this region differ from those observed elsewhere in the same basin, where environmental controls on the underlying availability of various food sources were likely quite different. These results highlight the complexities of dietary responses by hominins to changes in the availability of food resources.

'Remote' behavioural ecology: do megaherbivores consume vegetation in proportion to its presence in the landscape?

Examination of the feeding habits of mammalian species such as the African elephant (Loxodonta africana) that range over large seasonally dynamic areas is exceptionally challenging using field-based methods alone. Although much is known of their feeding preferences from field studies, conclusions, especially in relation to differing habits in wet and dry seasons, are often contradictory. Here, two remote approaches, stable carbon isotope analysis and remote sensing, were combined to investigate dietary changes in relation to tree and grass abundances to better understand elephant dietary choice in the Kruger National Park, South Africa. A composited pair of Landsat Enhanced Thematic Mapper satellite images characterising flushed and senescent vegetation states, typical of wet and dry seasons respectively, were used to generate land-cover maps focusing on the forest to grassland gradient. Stable carbon isotope analysis of elephant faecal samples identified the proportion of C3 (typically browse)/C4 (typically grass) in elephant diets in the 1-2 days prior to faecal deposition. The proportion of surrounding C4 land-cover was extracted using concentric buffers centred on faecal sample locations, and related to the faecal %C4 content. Results indicate that elephants consume C4 vegetation in proportion to its availability in the surrounding area during the dry season, but during the rainy season there was less of a relationship between C4 intake and availability, as elephants targeted grasses in these periods. This study illustrates the utility of coupling isotope and cost-free remote sensing data to conduct complementary landscape analysis at highly-detailed, biologically meaningful resolutions, offering an improved ability to monitor animal behavioural patterns at broad geographical scales. This is increasingly important due to potential impacts of climate change and woody encroachment on broad-scale landscape habitat composition, allowing the tracking of shifts in species utilisation of these changing landscapes in a way impractical using field based methods alone.

Saving Old Bones: a non-destructive method for bone collagen prescreening.

Bone collagen is an important material for radiocarbon, paleodietary, and paleoproteomic analyses, but it degrades over time, making such analyses more difficult with older material. Collagen preservation between and within archaeological sites is also variable, so that much time, effort, and money can go into the preparation and initial analysis of samples that will not yield meaningful results. To avoid this, various methods are employed to prescreen bone for collagen preservation (e.g., %N, microporosity, and FTIR spectroscopic analyses), but these are often destructive and/or require exportation for analysis. Here, we explore near-infrared spectroscopy as a tool for gauging the collagen content of ground and whole bone from about 500 to 45,000 years ago. We show that a portable spectrometer's ability to quantify collagen content and classify specimens by preservation status is comparable to that of other popular prescreening methods. Moreover, near-infrared spectroscopy is non-destructive and spectra can be acquired in a few seconds.

Seasonal and habitat effects on the nutritional properties of savanna vegetation: Potential implications for early hominin dietary ecology.

The African savannas that many early hominins occupied likely experienced stark seasonality and contained mosaic habitats (i.e., combinations of woodlands, wetlands, grasslands, etc.). Most would agree that the bulk of dietary calories obtained by taxa such as Australopithecus and Paranthropus came from the consumption of vegetation growing across these landscapes. It is also likely that many early hominins were selective feeders that consumed particular plants/plant parts (e.g., leaves, fruit, storage organs) depending on the habitat and season within which they were foraging. Thus, improving our understanding of how the nutritional properties of potential hominin plant foods growing in modern African savanna ecosystems respond to season and vary by habitat will improve our ability to model early hominin dietary behavior. Here, we present nutritional analyses (crude protein and acid detergent fiber) of plants growing in eastern and southern African savanna habitats across both wet and dry seasons. We find that many assumptions about savanna vegetation are warranted. For instance, plants growing in our woodland habitats have higher average protein/fiber ratios than those growing in our wetland and grassland transects. However, we find that the effects of season and habitat are complex, an example being the unexpectedly higher protein levels we observe in the grasses and sedges growing in our Amboseli wetlands during the dry season. Also, we find significant differences between the vegetation growing in our eastern and southern African field sites, particularly among plants using the C4 photosynthetic pathway. This may have implications for the differences we see between the stable carbon isotope compositions and dental microwear patterns of eastern and southern African Paranthropus species, despite their shared, highly derived craniodental anatomy.

Dietary Evolution: The Panda Paradox.

Giant pandas are specialized herbivores that digest little of the bamboo they consume. A new study argues that pandas, like carnivores, get most of their energy from protein, explaining their carnivore-like guts and poor digestion. This may have facilitated their ancestors' transition to herbivory.

The ecomorphology of southern African rodent incisors: Potential applications to the hominin fossil record.

The taxonomic identification of mammalian fauna within fossil assemblages is a well-established component of paleoenvironmental reconstructions. However, many fragmentary specimens recovered from fossil sites are often disregarded as they can be difficult to identify with the precision required for taxonomic methods. For this reason, the large numbers of isolated rodent incisors that are often recovered from hominin fossil bearing sites are generally regarded as offering little interpretive value. Ecomorphological analysis, often referred to as a "taxon-free" method, can potentially circumvent this problem by focusing on the adaptive, rather than the taxonomic significance of rodent incisor morphology. Here, we determine if the morphology of the upper incisors of modern southern African rodents reflects dietary behavior using discriminant function analysis. Our model suggests that a strong ecomorphological signal exists in our modern sample and we apply these results to two samples of isolated incisors from the hominin fossil bearing sites, Sterkfontein and Swartkrans.

Grass leaves as potential hominin dietary resources.

Discussions about early hominin diets have generally excluded grass leaves as a staple food resource, despite their ubiquity in most early hominin habitats. In particular, stable carbon isotope studies have shown a prevalent C4 component in the diets of most taxa, and grass leaves are the single most abundant C4 resource in African savannas. Grass leaves are typically portrayed as having little nutritional value (e.g., low in protein and high in fiber) for hominins lacking specialized digestive systems. It has also been argued that they present mechanical challenges (i.e., high toughness) for hominins with bunodont dentition. Here, we compare the nutritional and mechanical properties of grass leaves with the plants growing alongside them in African savanna habitats. We also compare grass leaves to the leaves consumed by other hominoids and demonstrate that many, though by no means all, compare favorably with the nutritional and mechanical properties of known primate foods. Our data reveal that grass leaves exhibit tremendous variation and suggest that future reconstructions of hominin dietary ecology take a more nuanced approach when considering grass leaves as a potential hominin dietary resource.

Dietary flexibility of Australopithecus afarensis in the face of paleoecological change during the middle Pliocene: Faunal evidence from Hadar, Ethiopia.

One approach to understanding the context of changes in hominin paleodiets is to examine the paleodiets and paleohabitats of contemporaneous mammalian taxa. Recent carbon isotopic studies suggest that the middle Pliocene was marked by a major shift in hominin diets, characterized by a significant increase in C4 foods in Australopithecus-grade species, including Australopithecus afarensis. To contextualize previous isotopic studies of A. afarensis, we employed stable isotopes to examine paleodiets of the mammalian fauna contemporaneous with A. afarensis at Hadar, Ethiopia. We used these data to inform our understanding of paleoenvironmental change through the deposition of the Hadar Formation. While the majority of the taxa in the Hadar fauna were C4 grazers, most show little change in the intensity of C4 food consumption over the 0.5 million-year interval sampled. Two taxa (equids and bovins) do show increases in C4 consumption through the Hadar Formation and into the younger, overlying Busidima Formation. Changes in the distributions of C4-feeders, C3-feeders and mixed-C3/C4-feeders in the sampled intervals are consistent with evidence of dietary reconstructions based on ecomorphology, and with habitats reconstructed using community structure analyses. Meanwhile, A. afarensis is one of many mammalian taxa whose C4 consumption does not show directional change over the intervals sampled. In combination with a wide range of carbon and oxygen isotopic composition for A. afarensis as compared to the other large mammal taxa, these results suggest that the C3/C4 dietary flexibility of A. afarensis was relatively unusual among most of its mammalian cohort.

The stable isotope ecology of Pan in Uganda and beyond.

Stable isotope analysis has long been used to study the dietary ecology of living and fossil primates, and there has been increasing interest in using stable isotopes to study primate habitat use and anthropogenic impacts on non-human primates. Here, we examine the stable carbon and nitrogen isotope compositions of chimpanzees (Pan troglodytes) from seven communities in Uganda across a continuum of habitat structure (closed to more open) and access to anthropogenic resources (no reliance to heavy reliance). In general, the hair δ(13) C, but not δ(15) N, values of these communities vary depending on forest structure and degree of anthropogenic influence. When integrated with previously published hair δ(13) C and δ(15) N values for Pan, it is apparent that modern "savanna" and "forest" Pan form discrete clusters in carbon and nitrogen isotope space, although there are exceptions probably relating to microhabitat specialization. The combined dataset also reveals that Pan δ(13) C values (but not δ(15) N values) are inversely related to rainfall (r(2) = 0.62). We converted Pan hair δ(13) C values to enamel equivalents and made comparisons to the fossil hominoids Sivapithecus sp., Gigantopithecus blacki, Ardipithecus ramidus, and Australopithecus anamensis. The δ(13) C values of the fossil hominins Ar. ramidus and Au. anamensis do not cluster with the δ(13) C values of modern Pan in "forest" habitats, or with fossil hominoids that are believed to have inhabited forests. Am. J. Primatol. 78:1070-1085, 2016. © 2016 Wiley Periodicals, Inc.

Advances in primate stable isotope ecology-Achievements and future prospects.

Stable isotope biogeochemistry has been used to investigate foraging ecology in non-human primates for nearly 30 years. Whereas early studies focused on diet, more recently, isotopic analysis has been used to address a diversity of ecological questions ranging from niche partitioning to nutritional status to variability in life history traits. With this increasing array of applications, stable isotope analysis stands to make major contributions to our understanding of primate behavior and biology. Most notably, isotopic data provide novel insights into primate feeding behaviors that may not otherwise be detectable. This special issue brings together some of the recent advances in this relatively new field. In this introduction to the special issue, we review the state of isotopic applications in primatology and its origins and describe some developing methodological issues, including techniques for analyzing different tissue types, statistical approaches, and isotopic baselines. We then discuss the future directions we envision for the field of primate isotope ecology. Am. J. Primatol. 78:995-1003, 2016. © 2015 Wiley Periodicals, Inc.

Stable isotopes (carbon, nitrogen, sulfur), diet, and anthropometry in urban Colombian women: investigating socioeconomic differences.

OBJECTIVES: We conducted stable isotope and dietary analyses of women from higher and lower socioeconomic status (SES) groups in Cali, Colombia. The objectives were to test between-group differences in stable isotope, dietary, and anthropometric characteristics, and to evaluate relationships between diet and stable isotope values. METHODS: Hair samples from 38 women (mean age 33.4) from higher and lower SES groups were analyzed for δ(13) C, δ(15) N, and δ(34) S values. Dietary intake was assessed via 24-h recalls. Anthropometric variables measured were body mass index, five body circumferences, and six skinfold thicknesses. RESULTS: Mean δ(13) C and δ(15) N values of the higher SES group (-16.4 and 10.3‰) were significantly greater than those of the lower SES group (-17.2 and 9.6‰; P < 0.01), but mean δ(34) S values did not differ significantly between groups (higher SES: 4.6‰; lower SES: 5.1‰). The higher SES group consumed a greater percentage of protein than the lower SES group (14% vs. 12% of energy; P = 0.03), but the groups did not differ in other dietary characteristics or in anthropometric characteristics. δ(13) C, δ(15) N, and δ(34) S values were not correlated with intake of the dietary items predicted (sugars, animal-source protein, and marine foods, respectively). The lower SES group was more variable in all three stable isotope values (P < 0.05), mirroring a trend toward greater dietary variability in this group. CONCLUSIONS: Stable isotope values revealed a difference between SES groups that was not explained by the dietary data. The relationship between diet and stable isotope composition is complex.

Intra-tooth stable isotope analysis of dentine: a step toward addressing selective mortality in the reconstruction of life history in the archaeological record.

Intra-tooth stable isotope analysis of dentine provides a more sensitive means to examine infant and childhood life history in the past than conventional cross-sectional analyses that rely on age-at-death. In addition, reconstructions of early diet and life history using an intra-tooth approach circumvent potential problems associated with mortality bias, which may operate strongly during infancy and childhood. We present new intra-tooth stable carbon and nitrogen isotope profiles in dentine collagen of early forming permanent teeth in a sample of adults from the Medieval Nubian site of Kulubnarti. We interpret the profiles in terms of weaning behavior and dietary history, and we compare profiles generated from first molars and canines to explore the degree to which these tooth types correspond. We then compare the profiles to the occurrence of linear enamel hypoplasia to assess the relationship between the timing of the weaning process and stress events. Finally, we compare the longitudinal profiles to cross-sectional stable isotope data obtained from rib collagen to investigate how life histories might differ between those that survived into adulthood and those that did not. Results suggest that canine and first molar profiles are in broad agreement, that hypoplastic stress events occurred during rather than before or after the weaning process in our sample, and that survivors appear to have weaned earlier than the average non-survivor. We suggest that this approach may be useful for addressing the effects of selective mortality on reconstructions of early life history and the relationship between early life history and morbidity.

Using the stable carbon and nitrogen isotope compositions of vervet monkeys (Chlorocebus pygerythrus) to examine questions in ethnoprimatology.

This study seeks to understand how humans impact the dietary patterns of eight free-ranging vervet monkey (Chlorocebus pygerythrus) groups in South Africa using stable isotope analysis. Vervets are omnivores that exploit a wide range of habitats including those that have been anthropogenically-disturbed. As humans encroach upon nonhuman primate landscapes, human-nonhuman primate interconnections become increasingly common, which has led to the rise of the field of ethnoprimatology. To date, many ethnoprimatological studies have examined human-nonhuman primate associations largely in qualitative terms. By using stable carbon (δ13C) and nitrogen (δ15N) isotope analysis, we use quantitative data to understand the degree to which humans impact vervet monkey dietary patterns. Based on initial behavioral observations we placed the eight groups into three categories of anthropogenic disturbance (low, mid, and high). Using δ13C and δ15N values we estimated the degree to which each group and each anthropogenically-disturbed category was consuming C4 plants (primarily sugar cane, corn, or processed foods incorporating these crops). δ13C values were significantly different between groups and categories of anthropogenic-disturbance. δ15N values were significantly different at the group level. The two vervet groups with the highest consumption of C4 plants inhabited small nature reserves, appeared to interact with humans only sporadically, and were initially placed in the mid level of anthropogenic-disturbance. However, further behavioral observations revealed that the high δ13C values exhibited by these groups were linked to previously unseen raiding of C4 crops. By revealing these cryptic feeding patterns, this study illustrates the utility of stable isotopes analysis for some ethnoprimatological questions.

Impacts of plant-based foods in ancestral hominin diets on the metabolism and function of gut microbiota in vitro.

UNLABELLED: Ancestral human populations had diets containing more indigestible plant material than present-day diets in industrialized countries. One hypothesis for the rise in prevalence of obesity is that physiological mechanisms for controlling appetite evolved to match a diet with plant fiber content higher than that of present-day diets. We investigated how diet affects gut microbiota and colon cells by comparing human microbial communities with those from a primate that has an extreme plant-based diet, namely, the gelada baboon, which is a grazer. The effects of potato (high starch) versus grass (high lignin and cellulose) diets on human-derived versus gelada-derived fecal communities were compared in vitro. We especially focused on the production of short-chain fatty acids, which are hypothesized to be key metabolites influencing appetite regulation pathways. The results confirmed that diet has a major effect on bacterial numbers, short-chain fatty acid production, and the release of hormones involved in appetite suppression. The potato diet yielded greater production of short-chain fatty acids and hormone release than the grass diet, even in the gelada cultures, which we had expected should be better adapted to the grass diet. The strong effects of diet on hormone release could not be explained, however, solely by short-chain fatty acid concentrations. Nuclear magnetic resonance spectroscopy found changes in additional metabolites, including betaine and isoleucine, that might play key roles in inhibiting and stimulating appetite suppression pathways. Our study results indicate that a broader array of metabolites might be involved in triggering gut hormone release in humans than previously thought. IMPORTANCE: One theory for rising levels of obesity in western populations is that the body's mechanisms for controlling appetite evolved to match ancestral diets with more low-energy plant foods. We investigated this idea by comparing the effects of diet on appetite suppression pathways via the use of gut bacterial communities from humans and gelada baboons, which are modern-day primates with an extreme diet of low-energy plant food, namely, grass. We found that diet does play a major role in affecting gut bacteria and the production of a hormone that suppresses appetite but not in the direction predicted by the ancestral diet hypothesis. Also, bacterial products were correlated with hormone release that were different from those normally thought to play this role. By comparing microbiota and diets outside the natural range for modern humans, we found a relationship between diet and appetite pathways that was more complex than previously hypothesized on the basis of more-controlled studies of the effects of single compounds.