A skew in poo: Biases in primate fecal isotope analysis and recommendations for standardized sample preparation.

Feces are a treasure trove in the study of animal behavior and ecology. Stable carbon and nitrogen isotope analysis allows to assess the dietary niches of elusive primate species and primate breastfeeding behavior. However, some fecal isotope data may unwillingly be biased toward the isotope ratios of undigested plant matter, requiring more consistent sample preparation protocols. We assess the impact of this potential data skew in 114 fecal samples of wild bonobos (Pan paniscus) by measuring the isotope differences (Δ13 C, Δ15 N) between bulk fecal samples containing larger particles (>1 mm) and filtered samples containing only small particles (<1 mm). We assess the influence of fecal carbon and nitrogen content (ΔC:N) and sample donor age (subadult, adult) on the resulting Δ13 C, Δ15 N values (n = 228). Additionally, we measure the isotope ratios in three systematically sieved fecal samples of chimpanzees (Pan troglodytes verus), with particle sizes ranging from 20 µm to 8 mm (n = 30). We found differences in fecal carbon and nitrogen content, with the smaller fecal fraction containing more nitrogen on average. While the Δ13 C values were small and not affected by age or ΔC:N, the Δ15 N values were significantly influenced by fecal ΔC:N, possibly resulting from the differing proportions of undigested plant macroparticles. Significant relationships between carbon stable isotope ratios (δ13 C) values and %C in large fecal fractions of both age groups corroborated this assessment. Δ15 N values were significantly larger in adults than subadults, which should be of concern in isotope studies comparing adult females with infants to assess breastfeeding. We found a random variation of up to 3.0‰ in δ13 C and 2.0‰ in nitrogen stable isotope ratios within the chimpanzee fecal samples separated by particle sizes. We show that particle size influences isotope ratios and propose a simple, cost-effective filtration method for primate feces to exclude larger undigested food particles from the analysis, which can easily be adopted by labs worldwide.

How isotopic signatures relate to meat consumption in wild chimpanzees: A critical reference study from Taï National Park, Côte d'Ivoire.

The roots of human hunting and meat eating lie deep in our evolutionary past shared with chimpanzees (Pan troglodytes). From the few habituated wild populations, we know that there is considerable variation in the extent to which chimpanzees consume meat. Expanding our knowledge of meat eating frequencies to more, yet unhabituated, populations requires noninvasive, indirect quantitative techniques. We here evaluate the use of stable isotopes to reconstruct meat-eating behavior in wild chimpanzees. We present hair isotope data (n = 260) of two western chimpanzee (P. troglodytes verus) groups from Taï forest (Côte d'Ivoire) and relate them to directly observed amounts of meat consumed, sex/female reproductive state, and group, while controlling for differences between individuals, seasons, and observation efforts. Succeeding seven months of hunting observations, we collected hair of 25 individuals for sequential analysis of δ15N and δ13C. Hunting success in the 7-month study period varied between the groups, with 25 successful hunts in the East group and only 8 in the North group. However, our models only found a direct relationship between amounts of meat consumed and variation within individual hair δ15N values in the East group, but not in the North group and not when comparing between individuals or groups. Although on average East group individuals consumed more than double the amount of meat than North group individuals, their δ15N values were significantly lower, suggesting that differences in microhabitat are substantial between group territories. The effect of sex/female reproductive state was significant in δ15N and δ13C, suggesting it related to access to food or feeding preferences. We conclude that several factors additional to diet are influencing and thus obscuring the isotope ratios in wild chimpanzee hair, particularly when comparing between sexes and social groups.

Seasonality and interindividual variation in mandrill feeding ecology revealed by stable isotope analyses of hair and blood.

Mandrills are large-bodied terrestrial forest primates living in particularly large social groups of several hundred individuals. Following these groups in the wild to assess differences in diet over time as well as among individuals is demanding. We here use isotope analyses in blood and hair obtained during repeated captures of 43 identified free-ranging mandrills (Mandrillus sphinx) from Southern Gabon, to test how dietary variation relates to the season as well as an individual's age and sex. We measured the stable carbon (δ13 C‰) and nitrogen (δ15 N‰) isotope ratios in 46 blood and 214 hair section samples as well as from a small selection of mandrill foods (n = 24). We found some seasonal isotopic effects, with lower δ13 C values but higher δ15 N values observed during the highly competitive long dry season compared to the fruit-rich long rainy season. Variation in δ13 C was further predicted by individual age, with higher δ13 C values generally found in younger individuals suggesting that they may consume more high canopy fruit than older individuals, or that older individuals consume more low canopy foliage. The best predictor for δ15 N values was the interaction between age and sex, with mature and reproductively active males revealing the highest δ15 N values, despite the observation that males consume substantially less animal food items than females. We interpret high δ15 N values in these mature male mandrill blood and hair sections to be the result of nutritional stress associated with intense male-male competition, particularly during mating season. This is the first study showing isotopic evidence for nutritional stress in a free-ranging primate species and may spark further investigations into male mandrill diet and energy balance.

Stable isotope variation in savanna chimpanzees (Pan troglodytes verus) indicate avoidance of energetic challenges through dietary compensation at the limits of the range.

OBJECTIVES: Food scarcity is proposed to be a limitation to chimpanzees at the limits of their range; however, such a constraint has never been investigated in this context. We investigated patterns of δ13 C and δ15 N variation along a latitudinal gradient at the northwestern West African chimpanzee (Pan troglodytes verus) range limit with the expectation that isotope ratios of chimpanzees at the range limit will indicate different dietary strategies or higher physiological constraints than chimpanzees further from the edge. MATERIALS AND METHODS: We measured δ13 C and δ15 N values in hair (n = 81) and plant food (n = 342) samples from five chimpanzee communities located along a latitudinal gradient in Southeastern Senegal. RESULTS: We found clear grouping patterns in hair δ13 C and δ15 N in the four southern sites compared to the northernmost site. Environmental baseline samples collected from these sites revealed overall higher plant δ15 N values at the northernmost site, but similar δ13 C values across sites. By accounting for environmental baseline, Δ13 C and Δ15 N values were clustered for all five sites relative to total Pan variation, but indicated a 13 C-enriched diet at the range limit. DISCUSSION: Clustering in Δ13 C and Δ15 N values supports that strategic shifting between preferred and fallback foods is a likely ubiquitous but necessary strategy employed by these chimpanzees to cope with their environment, potentially allowing chimpanzees at their limits to avoid periods of starvation. These results also underline the necessity of accounting for local isotopic baseline differences during inter-site comparison.

Comparative isotope ecology of African great apes.

The isotope ecology of great apes is a useful reference for palaeodietary reconstructions in fossil hominins. As extant apes live in C3-dominated habitats, variation in isotope signatures is assumed to be low compared to hominoids exploiting C4-plant resources. However, isotopic differences between sites and between and within individuals are poorly understood due to the lack of vegetation baseline data. In this comparative study, we included all species of free-ranging African great apes (Pan troglodytes, Pan paniscus, Gorilla sp.). First, we explore differences in isotope baselines across different habitats and whether isotopic signatures in apes can be related to feeding niches (faunivory and folivory). Secondly, we illustrate how stable isotopic variations within African ape populations compare to other extant and extinct primates and discuss possible implications for dietary flexibility. Using 701 carbon and nitrogen isotope data points resulting from 148 sectioned hair samples and an additional collection of 189 fruit samples, we compare six different great ape sites. We investigate the relationship between vegetation baselines and climatic variables, and subsequently correct great ape isotope data to a standardized plant baseline from the respective sites. We obtained temporal isotopic profiles of individual animals by sectioning hair along its growth trajectory. Isotopic signatures of great apes differed between sites, mainly as vegetation isotope baselines were correlated with site-specific climatic conditions. We show that controlling for plant isotopic characteristics at a given site is essential for faunal data interpretation. While accounting for plant baseline effects, we found distinct isotopic profiles for each great ape population. Based on evidence from habituated groups and sympatric great ape species, these differences could possibly be related to faunivory and folivory. Dietary flexibility in apes varied, but temporal variation was overall lower than in fossil hominins and extant baboons, shifting from C3 to C4-resources, providing new perspectives on comparisons between extinct and extant primates.

Reconstructing temporal variation in great ape and other primate diets: A methodological framework for isotope analyses in hair.

Stable isotope analysis of carbon and nitrogen in hair provides a versatile tool for reconstructing feeding behavior in elusive primate species. Particularly in great apes, researchers can sample long hair completely non-invasively from nests, allowing the investigation of inter- and intra-individual dietary variation. Given its incremental growth pattern, hair records temporal shifts in diet over long periods and allows one to reconstruct seasonal dietary patterns in species that cannot be directly observed. However, as for other sample materials, there are potential drawbacks related to the properties of hair keratin. Here I review some important facts on the nature of primate hair and also introduce new isotopic data from infant bonobo hair to provide methodological recommendations for future sample collection in the field and sample preparation in the laboratory. While these methodological guidelines focus on great apes which can be sampled strictly non-invasively, I also consider applications to other free-ranging primates. The biochemical composition, growth cycle, isotope turnover rate and isotopic fractionation in hair keratin are particularly relevant for data analysis and interpretation. Also, one can microscopically identify infant hairs and analyze them separately to study nursing and weaning behavior in primates. The goal of this article is to encourage primatologists to analyze the stable isotope ratios of hair to assess primate feeding ecology. Am. J. Primatol. 78:1004-1016, 2016. © 2015 Wiley Periodicals, Inc.

Who is who matters-The effects of pseudoreplication in stable isotope analyses.

Stable isotope analysis in free-ranging primates is a promising new avenue in reconstructing feeding niches and temporal dietary variation. Particularly, the large sample sizes obtained from non-invasively collected hair and fecal samples from nests of great apes offer great potential. However, analyzing repeated observations of the same individuals without controlling for potential differences among them means to "pseudoreplicate" and can lead to a greatly inflated probability of erroneous significance. We here test the effects of pseudoreplication in stable isotope data of great ape hair by means of simulations. We show that pseudoreplication can severely affect the probability of erroneous significance as well as non-significance. We suggest several strategies to avoid pseudoreplication in primate isotope ecology. First, if applicable, information on individual identity should be included in statistical analyses. Second, if samples derive from unhabituated animals, sampling at far apart locations or territories should avoid resampling of the same animal. In great apes, sampling of independent nests within nest groups can ensure that each sample derives from a different individual. Third, we encourage the combination of genetic surveys with sampling for isotope analyses to ensure the (genetic) identification of individuals. Am. J. Primatol. 78:1017-1030, 2016. © 2015 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.

Niche differentiation and dietary seasonality among sympatric gorillas and chimpanzees in Loango National Park (Gabon) revealed by stable isotope analysis.

The feeding ecology of sympatric great ape species yields valuable information for palaeodietary reconstructions in sympatric early hominin species. However, no isotopic references on sympatrically living apes and their feeding ecology are currently available. Here we present the first isotopic study on sympatric great apes, namely western lowland gorillas (Gorilla gorilla gorilla) and central chimpanzees (Pan troglodytes troglodytes) from Loango National Park, Gabon. We successfully analyzed the stable carbon and nitrogen isotope ratios in a selection of food plants (n = 31) and hair samples (n = 30) retrieved from sleeping nests to test whether niche partitioning among sympatric chimpanzees and gorillas is detectable using isotope analysis of hair. Ape hair strands with roots were sectioned into sequential segments (n = 100) to investigate temporal isotopic variation related to seasonal variations in food resources. We found significant δ(13)C differences between herbaceous plants and fruits, most likely due to canopy effects. While the δ(13)C values of chimpanzees indicate the consumption of fruit, the low δ(13)C values in gorilla hair indicate folivory, most likely the consumption of (13)C-depleted herbaceous vegetation. Our isotopic data also confirmed dietary overlap between chimpanzees and gorillas, which varied by season. Gorillas showed significant variation in δ(13)C values in response to season due to shifting proportions of herbaceous plants versus fruits. In chimpanzees, significant seasonal variation in δ(15)N was likely related to the seasonal availability of fruit species with particularly high δ(15)N values. In summary, we found isotopic evidence for niche partitioning and seasonal dietary variation among sympatric great apes at Loango. These findings provide a valuable reference for palaeodietary research on fossil hominins using δ(13)C analyses, particularly for studies focusing on sympatric taxa and on temporal isotopic variation within incremental tissues such as tooth enamel.

Exploring the contribution and significance of animal protein in the diet of bonobos by stable isotope ratio analysis of hair.

In primates, age, sex, and social status can strongly influence access to food resources. In Pan, these criteria are assumed to influence access to vertebrate meat. However, the significance of meat in terms of its role in the nutrition of Pan is still debated. Here we present a study using stable carbon and nitrogen isotope ratios in hair samples from habituated, wild bonobos (Pan paniscus) to explore these issues. Over a period of 5 mo hair samples were collected from fresh bonobo nests at LuiKotale, Democratic Republic of Congo. Hair samples were assigned to known individuals and were of sufficient length to allow the evaluation of isotopic variation over several months. Samples of plant foods and sympatric fauna were also analyzed. The δ(13)C and δ(15)N results of the bonobo hair were remarkably homogeneous over time and for the group as a whole. There are no differences in diet between the sexes. Within the group of males, however, there was a positive correlation between dominance status and δ(15)N. The isotopic data indicate that the contribution of fauna to bonobo diet is marginal and that plant food is the dietary protein source. In only some cases did elevated δ(15)N hair values correlate with observed faunivory and not correspond to the δ(15)N measured in the dominant plant foods. Given the large variation in hunting and meat eating of Pan across the African continent, the detection of seasonal changes in faunivory by elevated δ(15)N values in sectioned ape hair is a promising approach.

Strontium isotopes track female dispersal in Taï chimpanzees.

OBJECTIVES: Chimpanzees (Pan troglodytes) are patrilocal, with males remaining in their natal community and females dispersing when they reach sexual maturity. However, the details of female chimpanzee dispersal, such as their possible origin, are difficult to assess, even in habituated communities. This study investigates the utility of 87Sr/86Sr analysis for (1) assessing Sr baseline differences between chimpanzee territories and (2) identifying the status (immigrant or natal) of females of unknown origin within the territories of five neighboring communities in Taï National Park (Côte d'Ivoire). MATERIALS AND METHODS: To create a local Sr isoscape for the Taï Chimpanzee Project (TCP) study area, we sampled environmental samples from TCP-established territories (n = 35). To assess dispersal patterns, 34 tooth enamel samples (one per individual) were selected from the Taï chimpanzee skeletal collection. 87Sr/86Sr analysis was performed on all 69 samples at the W.M. Keck Lab. The theoretical density and overlap of chimpanzee communities as well as generalized linear mixed models (GLMMs) were used to test each question. RESULTS: 87Sr/86Sr ratios for natal male chimpanzees ranged from 0.71662 to 0.72187, which is well within the corresponding environmental baseline range of 0.70774-0.73460. The local Sr isoscapes fit was estimated with the root-mean-square error value, which was 0.0048 (22% of the whole 87Sr/86Sr data range). GLMMs identified significant differences in 87Sr/86Sr ratios between natal and unknown North community origin groups, suggesting that after 1980, females of unknown origin could be immigrants to North community (n = 7, z-ratio = -4.08, p = 0.0001, power = 0.94). DISCUSSION: This study indicates that 87Sr/86This study indicates that 87Sr/86Sr analysis can successfully identify immigrant females in skeletal collections obtained from wild chimpanzee communities, enabling the tracking of female dispersal patterns historically. There are, however, significant limitations within the scope of this study, such as (1) the absence of reliable maps for the TCP study area, (2) limited capacity for environmental sampling, (3) small sample sizes, and (4) tooth formation in wild chimpanzees.

Identification of energy consumption and nutritional stress by isotopic and elemental analysis of urine in bonobos (Pan paniscus).

A mounting body of evidence suggests that changes in energetic conditions like prolonged starvation can be monitored using stable isotope ratios of tissues such as bone, muscle, hair, and blood. However, it is unclear if urinary stable isotope ratios reflect a variation in energetic condition, especially if these changes in energetic condition are accompanied by shifts in dietary composition. In a feeding experiment conducted on captive bonobos (Pan paniscus), we monitored urinary δ(13)C, δ(15)N, total C (carbon), total N (nitrogen), and C/N ratios and compared these results with glucocorticoid levels under gradually changing energy availability and dietary composition. Measurements of daily collected urine samples over a period of 31 days showed that while shifts in urinary isotope signatures of δ(13)C and δ(15)N as well as total C were best explained by changes in energy consumption, urinary total N excretion as well as the C/N ratios matched the variation in dietary composition. Furthermore, when correcting for fluctuations in dietary composition, the isotope signatures of δ(13)C and δ(15)N as well as total C correlated with urinary glucocorticoid levels; however, the urinary total N and the C/N ratio did not. These results indicate for the first time that it is possible to non-invasively explore specific longitudinal records on animal energetic conditions and dietary compositions with urinary stable isotope ratios and elemental compositions, and this research provides a strong foundation for investigating how ecological factors and social dynamics affect feeding habits in wild animal populations such as primates.

Multi-isotopic analysis reveals individual mobility and diet at the Early Iron Age monumental tumulus of Magdalenenberg, Germany.

For the Early Iron Age western Hallstatt culture, which includes the site of Magdalenenberg in southwest Germany, it has been proposed that people were mobile and maintained far reaching social and trading networks throughout Europe. We tested this hypothesis by analyzing multiple isotopes (strontium, oxygen, sulfur, carbon, and nitrogen) of the preserved skeletons from the Magdalenenberg elite cemetery to determine diets and to look for evidence of mobility. The analysis of carbon, nitrogen, and sulfur isotope ratios in collagen of humans (n = 50) and associated domestic fauna (n = 10) indicates a terrestrial-based diet. There was a heterogeneous range of isotope values in both strontium (0.70725 to 0.71923, n = 76) and oxygen (13.4‰ to 18.5‰, n = 78) measured in tooth enamel. Although many of the individuals had values consistent with being from Hallstatt culture sites within southwest Germany, some individuals likely originated from further afield. Possible areas include the Alps of Switzerland and Austria or even locations in Italy. Our study strongly supports the assumption of far reaching social and economic networks in the western Hallstatt culture.

A Healthier Smile in the Past? Dental Caries and Diet in Early Neolithic Farming Communities from Central Germany.

Dental health is closely linked to an individual's health and diet. This bioarcheological study presents dental caries and stable isotope data obtained from prehistoric individuals (n = 101) from three Early Neolithic sites (c. 5500-4800 BCE) in central Germany. Dental caries and ante-mortem tooth loss (AMTL) were recorded and related to life history traits such as biological sex and age at death. Further, we correlate evidence on caries to carbon and nitrogen isotope data obtained from 83 individuals to assess the relationship between diet and caries. In 68.3% of the adults, carious lesions were present, with 10.3% of teeth affected. If AMTL is considered, the values increase by about 3%. The prevalence of subadults (18.4%) was significantly lower, with 1.8% carious teeth. The number of carious teeth correlated significantly with age but not sex. The isotopic data indicated an omnivorous terrestrial diet composed of domestic plants and animal derived protein but did not correlate with the prevalence of carious lesions. The combined evidence from caries and isotope analysis suggests a prevalence of starchy foods such as cereals in the diet of these early farmers, which aligns well with observations from other Early Neolithic sites but contrasts to Late Neolithic and Early Bronze Age populations in Germany.

A strontium isoscape for the Conchucos region of highland Peru and its application to Andean archaeology.

Strontium isotope (87Sr/86Sr) analysis of human skeletal remains is an important method in archaeology to examine past human mobility and landscape use. 87Sr/86Sr signatures of a given location are largely determined by the underlying bedrock, and these geology specific isotope signatures are incorporated into skeletal tissue through food and water, often permitting the differentiation of local and non-local individuals in past human populations. This study presents the results of a systematic survey of modern flora and fauna (n = 100) from 14 locations to map the bioavailable 87Sr/86Sr signatures of the Conchucos region, an area where the extent of geologic variability was previously unknown. We illustrate the necessity to examine the variation in 87Sr/86Sr values of the different geological formations available to human land use to document the range of possible local 87Sr/86Sr values. Within the Conchucos region we found significant variation in environmental 87Sr/86Sr values (0.7078-0.7214). The resulting isoscape represents the largest regionally specific bioavailable 87Sr/86Sr map (3,840 km2) to date for the Andes, and will serve as a baseline for future archaeological studies of human mobility in this part of the Peruvian highlands.

Limited evidence of C4 plant consumption in mound building Macrotermes termites from savanna woodland chimpanzee sites.

Stable isotope analysis is an increasingly used molecular tool to reconstruct the diet and ecology of elusive primates such as unhabituated chimpanzees. The consumption of C4 plant feeding termites by chimpanzees may partly explain the relatively high carbon isotope values reported for some chimpanzee communities. However, the modest availability of termite isotope data as well as the diversity and cryptic ecology of termites potentially consumed by chimpanzees obscures our ability to assess the plausibility of these termites as a C4 resource. Here we report the carbon and nitrogen isotope values from 79 Macrotermes termite samples from six savanna woodland chimpanzee research sites across equatorial Africa. Using mixing models, we estimated the proportion of Macrotermes C4 plant consumption across savanna woodland sites. Additionally, we tested for isotopic differences between termite colonies in different vegetation types and between the social castes within the same colony in a subset of 47 samples from 12 mounds. We found that Macrotermes carbon isotope values were indistinguishable from those of C3 plants. Only 5 to 15% of Macrotermes diets were comprised of C4 plants across sites, suggesting that they cannot be considered a C4 food resource substantially influencing the isotope signatures of consumers. In the Macrotermes subsample, vegetation type and caste were significantly correlated with termite carbon values, but not with nitrogen isotope values. Large Macrotermes soldiers, preferentially consumed by chimpanzees, had comparably low carbon isotope values relative to other termite castes. We conclude that Macrotermes consumption is unlikely to result in high carbon isotope values in either extant chimpanzees or fossil hominins.

Food mechanical properties and isotopic signatures in forest versus savannah dwelling eastern chimpanzees.

Chimpanzees are traditionally described as ripe fruit specialists with large incisors but relatively small postcanine teeth, adhering to a somewhat narrow dietary niche. Field observations and isotopic analyses suggest that environmental conditions greatly affect habitat resource utilisation by chimpanzee populations. Here we combine measures of dietary mechanics with stable isotope signatures from eastern chimpanzees living in tropical forest (Ngogo, Uganda) and savannah woodland (Issa Valley, Tanzania). We show that foods at Issa can present a considerable mechanical challenge, most saliently in the external tissues of savannah woodland plants compared to their tropical forest equivalents. This pattern is concurrent with different isotopic signatures between sites. These findings demonstrate that chimpanzee foods in some habitats are mechanically more demanding than previously thought, elucidating the broader evolutionary constraints acting on chimpanzee dental morphology. Similarly, these data can help clarify the dietary mechanical landscape of extinct hominins often overlooked by broad C3/C4 isotopic categories.

4000 years of human dietary evolution in central Germany, from the first farmers to the first elites.

Investigation of human diet during the Neolithic has often been limited to a few archaeological cultures or single sites. In order to provide insight into the development of human food consumption and husbandry strategies, our study explores bone collagen carbon and nitrogen isotope data from 466 human and 105 faunal individuals from 26 sites in central Germany. It is the most extensive data set to date from an enclosed geographic microregion, covering 4,000 years of agricultural history from the Early Neolithic to the Early Bronze Age. The animal data show that a variety of pastures and dietary resources were explored, but that these changed remarkably little over time. In the human δ15N however we found a significant increase with time across the different archaeological cultures. This trend could be observed in all time periods and archaeological cultures (Bell Beaker phenomenon excluded), even on continuously populated sites. Since there was no such trend in faunal isotope values, we were able largely to exclude manuring as the cause of this effect. Based on the rich interdisciplinary data from this region and archaeological period we can argue that meat consumption increased with the increasing duration of farming subsistence. In δ13C, we could not observe any clear increasing or decreasing trends during the archaeological time periods, either for humans or for animals, which would have suggested significant changes in the environment and landscape use. We discovered sex-related dietary differences, with males of all archaeological periods having higher δ15N values than females, and an age-related increasing consumption of animal protein. An initial decrease of δ15N-values at the age of 1-2 years reveals partial weaning, while complete weaning took place at the age of 3-4 years.

The Steady State Great Ape? Long Term Isotopic Records Reveal the Effects of Season, Social Rank and Reproductive Status on Bonobo Feeding Behavior.

Dietary ecology of extant great apes is known to respond to environmental conditions such as climate and food availability, but also to vary depending on social status and life history characteristics. Bonobos (Pan paniscus) live under comparatively steady ecological conditions in the evergreen rainforests of the Congo Basin. Bonobos are an ideal species for investigating influences of sociodemographic and physiological factors, such as female reproductive status, on diet. We investigate the long term dietary pattern in wild but fully habituated bonobos by stable isotope analysis in hair and integrating a variety of long-term sociodemographic information obtained through observations. We analyzed carbon and nitrogen stable isotopes in 432 hair sections obtained from 101 non-invasively collected hair samples. These samples represented the dietary behavior of 23 adult bonobos from 2008 through 2010. By including isotope and crude protein data from plants we could establish an isotope baseline and interpret the results of several general linear mixed models using the predictors climate, sex, social rank, reproductive state of females, adult age and age of infants. We found that low canopy foliage is a useful isotopic tracer for tropical rainforest settings, and consumption of terrestrial herbs best explains the temporal isotope patterns we found in carbon isotope values of bonobo hair. Only the diet of male bonobos was affected by social rank, with lower nitrogen isotope values in low-ranking young males. Female isotope values mainly differed between different stages of reproduction (cycling, pregnancy, lactation). These isotopic differences appear to be related to changes in dietary preference during pregnancy (high protein diet) and lactation (high energy diet), which allow to compensate for different nutritional needs during maternal investment.