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Following the first descriptions of culture in primates, widespread agreement has developed that the term can be applied to nonhumans as group-specific, socially learned behaviors. While behaviors such as those involving extractive tool use have been researched intensively, we propose that behaviors that are more subtle, less likely to be ecologically constrained, and more likely to be socially shaped, such as cultural forms of communication, provide compelling evidence of culture in nonhuman primates. Additionally, cultural forms of communication can provide novel insights into animal cognition such as the capacity for conformity, conventionalized meanings, arbitrariness in signal forms, and even symbolism. In this paper we focus on evidence from studies conducted on wild great apes. First, we provide a thorough review of what exactly we do know, and by extension don't know, about great ape cultural communication. We argue that detailed research on both vocal and gestural communication in wild great apes shows a more nuanced and variable repertoire than once assumed, with increasing support for group-specific variation. Second, we discuss the relevance of great ape cultural communication and its potential for illustrating evolutionary continuity for human-like cultural attributes, namely cumulative culture and symbolism. In sum, a concerted effort to examine cultural forms of communication in great apes could reveal novel evidence for cultural capacities that have thus far been heavily debated in the literature and can simultaneously contribute to an improved understanding of the complex minds of our closest living relatives.
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Paleoclimate reconstructions have enhanced our understanding of how past climates have shaped present-day biodiversity. We hypothesize that the geographic extent of Pleistocene forest refugia and suitable habitat fluctuated significantly in time during the late Quaternary for chimpanzees (Pan troglodytes). Using bioclimatic variables representing monthly temperature and precipitation estimates, past human population density data, and an extensive database of georeferenced presence points, we built a model of changing habitat suitability for chimpanzees at fine spatio-temporal scales dating back to the Last Interglacial (120,000 BP). Our models cover a spatial resolution of 0.0467° (approximately 5.19 km2 grid cells) and a temporal resolution of between 1000 and 4000 years. Using our model, we mapped habitat stability over time using three approaches, comparing our modeled stability estimates to existing knowledge of Afrotropical refugia, as well as contemporary patterns of major keystone tropical food resources used by chimpanzees, figs (Moraceae), and palms (Arecacae). Results show habitat stability congruent with known glacial refugia across Africa, suggesting their extents may have been underestimated for chimpanzees, with potentially up to approximately 60,000 km2 of previously unrecognized glacial refugia. The refugia we highlight coincide with higher species richness for figs and palms. Our results provide spatio-temporally explicit insights into the role of refugia across the chimpanzee range, forming the empirical foundation for developing and testing hypotheses about behavioral, ecological, and genetic diversity with additional data. This methodology can be applied to other species and geographic areas when sufficient data are available.
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Pan troglodytes , Refúgio de Vida Selvagem , Animais , Biodiversidade , Clima , Ecossistema , Variação Genética , FilogeografiaRESUMO
Animals use tools for communication relatively rarely compared to tool use for extractive foraging. We investigated the tool-use behaviour accumulative stone throwing (AST) in wild chimpanzees, who regularly throw rocks at trees, producing impact sounds and resulting in the aggregations of rocks. The function of AST remains unknown but appears to be communication-related. We conducted field experiments to test whether impact sounds produced by throwing rocks at trees varied according to the tree's properties. Specifically, we compared impact sounds of AST and non-AST tree species. We measured three acoustic descriptors related to intrinsic timbre quality, and found that AST tree species produced impact sounds that were less damped, with spectral energy concentrated at lower frequencies compared to non-AST tree species. Buttress roots in particular produced timbres with low-frequency energy (low spectral centroid) and slower signal onset (longer attack time). In summary, chimpanzees use tree species capable of producing more resonant sounds for AST compared to other tree species available.
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Pan troglodytes , Comportamento de Utilização de Ferramentas , Animais , ÁrvoresRESUMO
Wild chimpanzees regularly use tools, made from sticks, leaves, or stone, to find flexible solutions to the ecological challenges of their environment. Nevertheless, some studies suggest strong limitations in the tool-using capabilities of chimpanzees. In this context, we present the discovery of a newly observed tool-use behavior in a population of chimpanzees (Pan troglodytes verus) living in the Bakoun Classified Forest, Guinea, where a temporary research site was established for 15 months. Bakoun chimpanzees of every age-sex class were observed to fish for freshwater green algae, Spirogrya sp., from rivers, streams, and ponds using long sticks and twigs, ranging from 9 cm up to 4.31 m in length. Using remote camera trap footage from 11 different algae fishing sites within an 85-km2 study area, we found that algae fishing occurred frequently during the dry season and was non-existent during the rainy season. Chimpanzees were observed algae fishing for as little as 1 min to just over an hour, with an average duration of 9.09 min. We estimate that 364 g of Spirogyra algae could be retrieved in this time, based on human trials in the field. Only one other chimpanzee population living in Bossou, Guinea, has been described to customarily scoop algae from the surface of the water using primarily herbaceous tools. Here, we describe the new behavior found at Bakoun and compare it to the algae scooping observed in Bossou chimpanzees and the occasional variant reported in Odzala, Republic of the Congo. As these algae are reported to be high in protein, carbohydrates, and minerals, we hypothesize that chimpanzees are obtaining a nutritional benefit from this seasonally available resource.
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Comportamento Alimentar , Pan troglodytes , Comportamento de Utilização de Ferramentas , Animais , Congo , Guiné , Microalgas , Estações do AnoRESUMO
BACKGROUND: Assessing the range and territories of wild mammals traditionally requires years of data collection and often involves directly following individuals or using tracking devices. Indirect and non-invasive methods of monitoring wildlife have therefore emerged as attractive alternatives due to their ability to collect data at large spatiotemporal scales using standardized remote sensing technologies. Here, we investigate the use of two novel passive acoustic monitoring (PAM) systems used to capture long-distance sounds produced by the same species, wild chimpanzees (Pan troglodytes), living in two different habitats: forest (Taï, Côte d'Ivoire) and savanna-woodland (Issa valley, Tanzania). RESULTS: Using data collected independently at two field sites, we show that detections of chimpanzee sounds on autonomous recording devices were predicted by direct and indirect indices of chimpanzee presence. At Taï, the number of chimpanzee buttress drums detected on recording devices was positively influenced by the number of hours chimpanzees were seen ranging within a 1 km radius of a device. We observed a similar but weaker relationship within a 500 m radius. At Issa, the number of indirect chimpanzee observations positively predicted detections of chimpanzee loud calls on a recording device within a 500 m but not a 1 km radius. Moreover, using just seven months of PAM data, we could locate two known chimpanzee communities in Taï and observed monthly spatial variation in the center of activity for each group. CONCLUSIONS: Our work shows PAM is a promising new tool for gathering information about the ranging behavior and habitat use of chimpanzees and can be easily adopted for other large territorial mammals, provided they produce long-distance acoustic signals that can be captured by autonomous recording devices (e.g., lions and wolves). With this study we hope to promote more interdisciplinary research in PAM to help overcome its challenges, particularly in data processing, to improve its wider application.
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How populations adapt to their environment is a fundamental question in biology. Yet we know surprisingly little about this process, especially for endangered species such as non-human great apes. Chimpanzees, our closest living relatives, are particularly interesting because they inhabit diverse habitats, from rainforest to woodland-savannah. Whether genetic adaptation facilitates such habitat diversity remains unknown, despite having wide implications for evolutionary biology and conservation. Using 828 newly generated exomes from wild chimpanzees, we find evidence of fine-scale genetic adaptation to habitat. Notably, adaptation to malaria in forest chimpanzees is mediated by the same genes underlying adaptation to malaria in humans. This work demonstrates the power of non-invasive samples to reveal genetic adaptations in endangered populations and highlights the importance of adaptive genetic diversity for chimpanzees.
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Bioacoustic research spans a wide range of biological questions and applications, relying on identification of target species or smaller acoustic units, such as distinct call types. However, manually identifying the signal of interest is time-intensive, error-prone, and becomes unfeasible with large data volumes. Therefore, machine-driven algorithms are increasingly applied to various bioacoustic signal identification challenges. Nevertheless, biologists still have major difficulties trying to transfer existing animal- and/or scenario-related machine learning approaches to their specific animal datasets and scientific questions. This study presents an animal-independent, open-source deep learning framework, along with a detailed user guide. Three signal identification tasks, commonly encountered in bioacoustics research, were investigated: (1) target signal vs. background noise detection, (2) species classification, and (3) call type categorization. ANIMAL-SPOT successfully segmented human-annotated target signals in data volumes representing 10 distinct animal species and 1 additional genus, resulting in a mean test accuracy of 97.9%, together with an average area under the ROC curve (AUC) of 95.9%, when predicting on unseen recordings. Moreover, an average segmentation accuracy and F1-score of 95.4% was achieved on the publicly available BirdVox-Full-Night data corpus. In addition, multi-class species and call type classification resulted in 96.6% and 92.7% accuracy on unseen test data, as well as 95.2% and 88.4% regarding previous animal-specific machine-based detection excerpts. Furthermore, an Unweighted Average Recall (UAR) of 89.3% outperformed the multi-species classification baseline system of the ComParE 2021 Primate Sub-Challenge. Besides animal independence, ANIMAL-SPOT does not rely on expert knowledge or special computing resources, thereby making deep-learning-based bioacoustic signal identification accessible to a broad audience.
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Aprendizado Profundo , Animais , Humanos , Aprendizado de Máquina , Algoritmos , Acústica , Área Sob a CurvaRESUMO
Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.
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Noninvasive samples as a source of DNA are gaining interest in genomic studies of endangered species. However, their complex nature and low endogenous DNA content hamper the recovery of good quality data. Target capture has become a productive method to enrich the endogenous fraction of noninvasive samples, such as faeces, but its sensitivity has not yet been extensively studied. Coping with faecal samples with an endogenous DNA content below 1% is a common problem when prior selection of samples from a large collection is not possible. However, samples classified as unfavourable for target capture sequencing might be the only representatives of unique specific geographical locations, or to answer the question of interest. To explore how library complexity may be increased without repeating DNA extractions and generating new libraries, in this study we captured the exome of 60 chimpanzees (Pan troglodytes) using faecal samples with very low proportions of endogenous content (<1%). Our results indicate that by performing additional hybridizations of the same libraries, the molecular complexity can be maintained to achieve higher coverage. Also, whenever possible, the starting DNA material for capture should be increased. Finally, we specifically calculated the sequencing effort needed to avoid exhausting the library complexity of enriched faecal samples with low endogenous DNA content. This study provides guidelines, schemes and tools for laboratories facing the challenges of working with noninvasive samples containing extremely low amounts of endogenous DNA.
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Exoma , Genômica , Hibridização de Ácido Nucleico , Animais , Fezes , Biblioteca Gênica , Sequenciamento de Nucleotídeos em Larga Escala , Pan troglodytes/genética , Análise de Sequência de DNARESUMO
Understanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution. IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.
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Much like humans, chimpanzees occupy diverse habitats and exhibit extensive behavioural variability. However, chimpanzees are recognized as a discontinuous species, with four subspecies separated by historical geographic barriers. Nevertheless, their range-wide degree of genetic connectivity remains poorly resolved, mainly due to sampling limitations. By analyzing a geographically comprehensive sample set amplified at microsatellite markers that inform recent population history, we found that isolation by distance explains most of the range-wide genetic structure of chimpanzees. Furthermore, we did not identify spatial discontinuities corresponding with the recognized subspecies, suggesting that some of the subspecies-delineating geographic barriers were recently permeable to gene flow. Substantial range-wide genetic connectivity is consistent with the hypothesis that behavioural flexibility is a salient driver of chimpanzee responses to changing environmental conditions. Finally, our observation of strong local differentiation associated with recent anthropogenic pressures portends future loss of critical genetic diversity if habitat fragmentation and population isolation continue unabated.
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Comportamento Animal , Evolução Molecular , Variação Genética , Componentes Genômicos , Repetições de Microssatélites , Pan troglodytes/genética , Migração Animal , Animais , Ecossistema , Interação Gene-Ambiente , Genética Populacional , Pan troglodytes/psicologia , Filogenia , Especificidade da EspécieRESUMO
Human ethnographic knowledge covers hundreds of societies, whereas chimpanzee ethnography encompasses at most 15 communities. Using termite fishing as a window into the richness of chimpanzee cultural diversity, we address a potential sampling bias with 39 additional communities across Africa. Previously, termite fishing was known from eight locations with two distinguishable techniques observed in only two communities. Here, we add nine termite-fishing communities not studied before, revealing 38 different technical elements, as well as community-specific combinations of three to seven elements. Thirty of those were not ecologically constrained, permitting the investigation of chimpanzee termite-fishing culture. The number and combination of elements shared among individuals were more similar within communities than between them, thus supporting community-majority conformity via social imitation. The variation in community-specific combinations of elements parallels cultural diversity in human greeting norms or chopstick etiquette. We suggest that termite fishing in wild chimpanzees shows some elements of cumulative cultural diversity.
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Diversidade Cultural , Comportamento Social , Animais , Pan troglodytesRESUMO
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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Large brains and behavioural innovation are positively correlated, species-specific traits, associated with the behavioural flexibility animals need for adapting to seasonal and unpredictable habitats. Similar ecological challenges would have been important drivers throughout human evolution. However, studies examining the influence of environmental variability on within-species behavioural diversity are lacking despite the critical assumption that population diversification precedes genetic divergence and speciation. Here, using a dataset of 144 wild chimpanzee (Pan troglodytes) communities, we show that chimpanzees exhibit greater behavioural diversity in environments with more variability - in both recent and historical timescales. Notably, distance from Pleistocene forest refugia is associated with the presence of a larger number of behavioural traits, including both tool and non-tool use behaviours. Since more than half of the behaviours investigated are also likely to be cultural, we suggest that environmental variability was a critical evolutionary force promoting the behavioural, as well as cultural diversification of great apes.
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Comportamento Animal , Pan troglodytes/psicologia , Animais , Ecossistema , Meio Ambiente , Feminino , Florestas , Masculino , Pan troglodytes/fisiologia , Comportamento de Utilização de FerramentasRESUMO
Hand-clapping is a form of gestural communication commonly observed in captive great apes yet only isolated instances of this behaviour have been documented in the wild. Nearly 20 years ago Fay recorded the first observations of hand-clapping in western lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic. Here we present observations of Likouala swamp gorillas using hand-clapping as a form of gestural communication in previously undocumented contexts in the wild. We observed hand-clapping on four different occasions in four different groups. The hand-clap was always exhibited by an adult female and always consisted of two consecutive claps conducted in front of the body. We suggest the functional significance of the behaviour was to maintain and enforce group cohesiveness during instances of alarm. These observations suggest western lowland gorillas have a means of communicating that is thus far absent in their eastern counterparts (Gorilla beringei ssp.). This could be a gestural culture found only in western lowland gorillas which should be investigated further to shed light on the evolution of communication among hominoids.
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Comunicação Animal , Gorilla gorilla/fisiologia , Mãos/fisiologia , Comportamento Social , Animais , Congo , Feminino , ObservaçãoRESUMO
Garcia and Dunn [1] raise some interesting and valuable points regarding our recent paper in Current Biology[2]. As Garcia and Dunn [1] point out, cross-species variation in vocal and anatomical relations allows for the identification of relevant outliers from the body size - fundamental frequency (f0) regression. However, this depends on the premise that the chosen or available f0 and body size values are typical of the species. A motivation for our study [2] was in part to improve the accuracy of such estimates by providing more data per species compared to previous studies. We address each point of their critique by controlling for cross-species body size variation using body weights for chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), addressing potential call variation in different subspecies of Pan troglodytes, measuring minimum f0 as well as maximum f0 and possible effects caused by different larynx fixation methods.
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Laringe , Pan paniscus , Animais , Pan troglodytesRESUMO
Temperament and personality research in humans and nonhuman animals measures behavioral variation in individual, population, or species-specific traits with implications for survival and fitness, such as social status, foraging, and mating success [1-5]. Curiosity and risk-taking tendencies have been studied extensively across taxa by measuring boldness and exploration responses to experimental novelty exposure [3, 4, 6-15]. Here, we conduct a natural field experiment using wildlife monitoring technology to test variation in the reaction of wild great apes (43 groups of naive chimpanzees, bonobos, and western gorillas across 14 field sites in Africa) to a novel object, the camera trap. Bonobo and gorilla groups demonstrated a stronger looking impulse toward the camera trap device compared to chimpanzees, suggesting higher visual attention and curiosity. Bonobos were also more likely to show alarm and other fearful behaviors, although such neophobic (and conversely, neophilic) responses were generally rare. Among all three species, individuals looked at cameras longer when they were young, were associating with fewer individuals, and did not live near a long-term research site. Overall, these findings partially validate results from great ape novelty paradigms in captivity [7, 8]. We further suggest that species-typical leadership styles [16] and social and environmental effects, including familiarity with humans, best explain novelty responses of wild great apes. In sum, this study illustrates the feasibility of large-scale field experiments and the importance of both intrinsic and extrinsic factors in shaping animal curiosity. VIDEO ABSTRACT.
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Comportamento Exploratório , Gorilla gorilla/psicologia , Pan paniscus/psicologia , Pan troglodytes/psicologia , Fotografação/instrumentação , África , Animais , Feminino , Masculino , Especificidade da EspécieRESUMO
Loud calls are used by many species as long-distance signals for group defense, mate attraction, and inter- and intragroup spacing. Chimpanzee loud calls, or pant hoots, are used in a variety of contexts including group coordination and during male contests. Here, we observed an alpha male takeover in wild chimpanzees (Pan troglodytes verus) during which the leaf clipping gesture re-emerged after disappearing for almost two years in this community. Leaf clipping only occurred in males and was observed almost exclusively prior to pant hoot vocalizations, as has been observed in other chimpanzee communities of the Taï forest in Côte d'Ivoire. Consequently, we hypothesized that leaf clipping may be important for male-male competition by affecting variation in the acoustic properties of male chimpanzee loud calls. We therefore investigated whether pant hoots preceded by leaf clipping differed acoustically from those without, while also testing the influence of social context on pant hoot variation, namely male dominance rank and hierarchy instability, i.e., before, during and after the alpha takeover. We found that pant hoots preceded by leaf clipping were longer, contained more call elements and drum beats, and lower fundamental and peak frequencies. Moreover, during the alpha takeover pant hoots were shorter, contained fewer drum beats and higher fundamental frequencies. Additionally, pant hoot and aggression rates were also highest during the alpha takeover with leaf clipping more likely to occur on days when pant hooting rates were high. Overall social rank had limited effects on pant hoot variation. We suggest that elevated arousal and aggression during the alpha takeover triggered the re-emergence of leaf clipping and the associated acoustic changes in pant hoots. Further research should focus on the potential mechanisms by which leaf clipping is connected to variation in pant hoots and cross-population comparisons of the behaviour.
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Acoustic signals, shaped by natural and sexual selection, reveal ecological and social selection pressures [1]. Examining acoustic signals together with morphology can be particularly revealing. But this approach has rarely been applied to primates, where clues to the evolutionary trajectory of human communication may be found. Across vertebrate species, there is a close relationship between body size and acoustic parameters, such as formant dispersion and fundamental frequency (f0). Deviations from this acoustic allometry usually produce calls with a lower f0 than expected for a given body size, often due to morphological adaptations in the larynx or vocal tract [2]. An unusual example of an obvious mismatch between fundamental frequency and body size is found in the two closest living relatives of humans, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although these two ape species overlap in body size [3], bonobo calls have a strikingly higher f0 than corresponding calls from chimpanzees [4]. Here, we compare acoustic structures of calls from bonobos and chimpanzees in relation to their larynx morphology. We found that shorter vocal fold length in bonobos compared to chimpanzees accounted for species differences in f0, showing a rare case of positive selection for signal diminution in both bonobo sexes.
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Laringe/anatomia & histologia , Pan paniscus/anatomia & histologia , Pan troglodytes/anatomia & histologia , Vocalização Animal , Acústica , Animais , Pan paniscus/fisiologia , Pan troglodytes/fisiologia , Especificidade da EspécieRESUMO
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.