Old age variably impacts chimpanzee engagement and efficiency in stone tool use

Senescence can be understood as a reduction in the efficacy of biological systems with increasing age. In recent decades, the senescence of non-human primates (henceforth primates) has been a point of considerable research interest (Colman, 2018; Edler et al., 2021; Gilleard, 2023). In part, this is due to the fact that primates offer uniquely translatable models for understanding the nature and evolution of human senescence, given their high genetic, physiological, and behavioral similarities (Colman, 2018; Bizon and Woods, 2009; Frye et al., 2022; Lane, 2000). Accordingly, many parallels between the senescent processes of humans and primates have been uncovered, including in their cognition (Comrie et al., 2018; Gray and Barnes, 2019; Herndon and Lacreuse, 2002; Lacreuse et al., 2014; Lacreuse et al., 2018; Lacreuse et al., 2020) physiology (Colman, 2018; Colman and Binkley, 2002; Didier et al., 2016; Lowenstine et al., 2016), and their resultant behaviors (Havercamp et al., 2021; Hozer et al., 2019; Neal Webb et al., 2019; Tarou et al., 2002; Zhdanova et al., 2011). However, thus far, the majority of these studies have focused on captive populations of short-living species and exploited existing variation in age among individuals to infer the effects of senescence through cross-sectional analyses (Colman, 2018; Gray and Barnes, 2019; Rothwell et al., 2021; Tardif and Ross, 2021). Comparatively, few studies have investigated how senescence influences the behaviors of primates in the wild (with the exception of a handful of examples Fujisawa et al., 2010; Newman et al., 2023; Siracusa et al., 2022b; Siracusa et al., 2024; Thompson et al., 2020), and even fewer employ longitudinal data sampling to understand how senescence leads to changes in the behaviors of specific individuals over time. These studies of wild individuals are highly valuable as they shed light on how aging affects the day-to-day behaviors that primates rely on for survival – conclusions which cannot be easily predicted from studies from captivity, given that patterns of physiological senescence can differ significantly between captive and naturalistic environments (Cole et al., 2024; Campos et al., 2024). Further research is therefore required to understand how aging influences the lives of wild primates. This is particularly true for long-living great ape species, which are underrepresented in the existing literature, yet their phylogenetic proximity to humans means that they likely offer the most suitable models for understanding the evolution of the human aging process.

Of the day-to-day behaviors of great apes, the combined physical and cognitive demands of tool use make it likely to exhibit particular changes with progressive old age. The tool-use behaviors of great apes are highly challenging, requiring tool users to draw upon a wide array of high-level cognitive abilities, including planning and the flexible assembly of actions into goal-directed behaviors (Byrne et al., 2013; Call, 2013; Carvalho et al., 2008; Howard-Spink et al., 2024); an understanding of causal relationships between objects (Hayashi, 2015; Matsuzawa, 1996; Sanz and Morgan, 2010); as well as knowledge of the physical properties of objects and how to exploit these properties to use tools successfully (Carvalho et al., 2008; Boesch and Boesch, 1983; Bril et al., 2009; Sirianni et al., 2015). Many of these cognitive abilities – including the more specific subcomponents of these abilities, such as motor coordination (Lacreuse et al., 2014), working memory (Glavis-Bloom et al., 2022), executive functioning (Lacreuse et al., 2020), and cognitive flexibility (Lacreuse et al., 2018) – have been identified as at risk of senescence in captive living primates; however, never in tool-use behaviors themselves. Moreover, physiological changes including reduced bone mass (Colman and Binkley, 2002; Lowenstine et al., 2016; Nichols and Zihlman, 2002), muscle wasting (sarcopenia; Lowenstine et al., 2016; Cann, 2015; Morbeck et al., 2002), the development of arthritis (Lowenstine et al., 2016), and reduced visual acuity (Fujisawa et al., 2010) have been identified in a number of primate species, including within the great apes, which all influence individual strength, dexterity, and accuracy of movement. These findings suggest that tool use could be a domain of great-ape behavior that is at specific risk of senescence; however, it has not yet been possible to address this question due to an absence of long-term data on great ape tool-use behaviors that also include instances of tool use performed by elderly individuals.

To address this gap in the literature, we used a longitudinal archive of video footage of wild, West African chimpanzees (Pan troglodytes verus) using stone tools to crack hard-shelled nuts as part of a decades-long field experiment in a clearing in the Bossou forest, Guinea (Matsuzawa et al., 2011; Sugiyama, 1981) ('the outdoor laboratory'; see Methods and Figure 1 for information about the experimental set up at the outdoor laboratory). Nut cracking is one of the most sophisticated forms of tool use observed in the animal kingdom, and is habitually performed by a number of primate species in the wild including several communities of chimpanzees (Pan troglodytes; Boesch and Boesch, 1983; Carvalho and McGrew, 2012; Matsuzawa, 1994), capuchin monkeys (Cebus and Sapajus spp.; Falótico et al., 2019; Fragaszy et al., 2023; Falótico et al., 2024; Goldsborough et al., 2024; Goldsborough et al., 2025), and long-tailed macaques (Macaca fascicularis; Luncz et al., 2019; Proffitt et al., 2018). During nut cracking, a nut is placed on a hard substrate for the chimpanzee population used in this study, this substrate is a portable anvil stone, although at other sites this may be a root or rocky outcrop (Boesch and Boesch, 1983; Sirianni et al., 2015), before being struck repeatedly with a hammer stone until the nut is cracked open and the edible kernel inside extracted and consumed (see Figure 1a). Nut cracking is learnt by chimpanzees at Bossou by the age of 7 years (often between 3.5 and 5 years of age; Biro et al., 2006; Inoue-Nakamura and Matsuzawa, 1997), and chimpanzees continue to perform this behavior throughout adulthood (Matsuzawa et al., 2011). This extended engagement in nut cracking permits characterization of how individual chimpanzees perform this behavior across their lives (Berdugo et al., 2025), including during the oldest years of their lifespan. Nut cracking features all of the key elements of tool-use behaviors which we predict will make them likely to senesce with old age, including the need to construct complex object associations (Hayashi, 2015; Matsuzawa, 1991; Matsuzawa, 1996) to organize and address multiple goals using an extended behavioral sequence (Carvalho et al., 2008; Howard-Spink et al., 2024) to select tool objects based on perceived properties (Carvalho et al., 2008; Boesch and Boesch, 1983; Sirianni et al., 2015), and to combine objects with sufficient dexterity, precision and force and to crack nuts without knocking nuts off the anvil, or smashing interior kernels (Bril et al., 2009).

Figure 1

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To determine whether – and if so, how – old age influenced the nut-cracking behaviors of wild chimpanzees, we sampled video footage collected at the outdoor laboratory in five field seasons spanning a 17-year timeframe between 1999 and 2016. During this timeframe, we collected longitudinal data on five chimpanzees as they aged from approximately 39–44 years old (end of mid-life) to 56–61 years old (ages which are close to the maximum for wild chimpanzee lifespans; Wood et al., 2023). Across sampled field seasons, we estimated how readily chimpanzees engaged in nut cracking behaviors using two key metrics: the frequency with which chimpanzees visited outdoor laboratory sites during each field season (compared to a control group of younger individuals between the ages of 8 and 30 years of age), and when present, the proportion of time chimpanzees spent engaging with nuts and stone tools compared to other key behaviors (such as drinking water from an available water point using leaf tools (Sousa et al., 2009) and eating oil-palm fruits that are provisioned alongside nuts; see Figure 1b and c). We also measured how quickly chimpanzees selected stone tools from a central matrix of over 50 stones (a generalized metric of efficiency during tool selection; see Figure 1d and e), as well as how efficiently chimpanzees cracked open nuts using stone tools and consumed the associated kernel.

Overall, with increasingly old age (measured by progressive field seasons), elderly chimpanzees were significantly less likely to visit experimental nut-cracking sites. In comparison, younger individuals (i.e. younger adults and older immatures who had learnt how to crack nuts) exhibited no change over successive field seasons, suggesting that this reduced attendance at experimental nut cracking sites was confined to an elderly, aging cohort of chimpanzees. When present at the outdoor laboratory, two of our five elderly individuals spent substantially less time engaging in nut cracking at older ages, as compared to their behaviors in previous field seasons. Moreover, several elderly chimpanzees took more time to select stone tools in later field seasons than in earlier field seasons, and were also less efficient at using stone tools to crack open oil-palm nuts. Importantly, we detected considerable interindividual variability in the effects of aging on how readily elderly chimpanzees engaged with nuts and stone tools, how quickly they selected tools, and the efficiency with which elderly chimpanzees used tools. Some individuals demonstrated little-to-no change in engagement and efficiency with aging, whereas others experienced significant changes across different aspects of their nut-cracking behavior. We discuss our findings in the context of existing literature for primate aging and hypothesize which factors underpin observed changes in behavior, including cognitive, physiological, and motivational causes, and generate a number of suggested avenues for further study. We also discuss how aging can likely compound existing interindividual differences in the proficiency of socially-learnt technical skills in non-human animals, and discuss how tool use could potentially present a suitable indicator for identifying individuals who are experiencing the effects of profound senescence in the wild.

We provide the first account of how a tool-use behavior performed by wild chimpanzees changed with progressively older age. Across a seventeen-year window, during which chimpanzees aged from 39-44 years to 56–61 years old, elderly chimpanzees began visiting experimental nut-cracking sites less frequently. This change in attendance rate was not observed for younger chimpanzees and was therefore confined to individuals who were approaching their maximum age in the wild. In addition, when present at nut cracking sites, two individuals (Fana and Velu) exhibited a lower engagement with nuts and stone tools in 2011 (the latest field season for this analysis) as compared with their behavior in earlier field seasons. With progressive aging, three individuals took longer to select stone tools (Yo, Fana, and Jire), several individuals took longer to crack open oil-palm nuts and consume all of the kernel, and two individuals (Yo and Velu) cracked and processed oil-palm nuts using a greater number of actions, including more frequent strikes of the hammer stone. Across metrics of engagement and efficiency, we detected interindividual differences in the extent to which nut cracking behaviors changed with progressive aging, including some individuals who exhibited little-to-no change in behavior across the time period sampled (see Table 2). Overall, our results provide initial evidence that elderly wild chimpanzees are subject to variable effects of aging on their habitual stone tool-use behaviors.

Whilst the outdoor laboratory locations are experimentally created nut-cracking sites, previous research on the performance of nut cracking across the home range at Bossou established that chimpanzees visit the outdoor laboratory at rates comparable to naturally occurring sites (Almeida-Warren et al., 2022), meaning that for most individuals at Bossou, the outdoor laboratory is a readily visited site for foraging. However, at progressively older ages, elderly chimpanzees began to visit the outdoor laboratory less frequently. This result was not found for younger chimpanzees between the ages of 8 and 30 years old, suggesting that changes in elderly chimpanzees’ attendance rates were not an artefact of environmental changes over field seasons (which would likely affect both age cohorts similarly).

In addition, by 2011, two elderly chimpanzees (Velu and Fana) engaged with nuts and stone tools less frequently than they had done during visits to the outdoor laboratory throughout earlier years (although note for Velu, data for 2011 were collected from a single encounter). The possible causes for these changes in attendance rate – and engagement with nuts and stone tools when present at the outdoor laboratory – are manifold. Firstly, physiological changes with aging – such as in metabolism and nutrient requirements – could influence individuals’ dietary preferences, reducing the appeal of nuts as an available food source. Secondly, physical senescence may make visiting nut cracking sites more challenging for elderly individuals, such as through reduced capacity for locomotion. Changes in locomotion have been documented in aging captive apes (Neal Webb et al., 2019). In the context of wild apes, reduced mobility may further restrict the available area that elderly chimpanzees can traverse during daily ranging, encouraging them to visit foraging patches that are more proximal to their immediate locations than the outdoor laboratory. Chimpanzees habitually plan their routes towards tool-use sites (Almeida-Warren et al., 2022); however, the extent to which their doing so changes during old age is unclear. Thirdly, it is possible that tool use may become more challenging due to changes in elderly chimpanzees’ cognitive or physical condition (see latter sections of our discussion), which may reduce the appeal of visiting nut-cracking sites. Fourthly, changes in social association may have influenced the likelihood that elderly chimpanzees visited experimental nut-cracking sites. When experiencing increasingly old ages, many primates (Neal Webb et al., 2019; Siracusa et al., 2022b; Campos et al., 2024; Almeling et al., 2016; Machanda and Rosati, 2020) – and other mammals (Siracusa et al., 2022a; Rudd et al., 2024; Albery et al., 2022) – display higher social selectivity and spend a greater proportion of their time either in isolation or in smaller group associations. This social aging arguably may not be senescence per se, but can either be the result of senescent processes (perhaps even exacerbating senescence; Siracusa et al., 2022a), or may act to benefit individuals experiencing senescence, such as reducing the risk of injury from antagonistic interactions with social partners, or by shielding oneself from contagious disease (Siracusa et al., 2022a; Siracusa et al., 2024). In the context of our study, chimpanzees at Bossou typically arrive at the outdoor laboratory when travelling in groups, and therefore party members may be led to nut-cracking sites by associated conspecifics, rather than through independent choice. Previous research has demonstrated that whilst gregariousness appears to be constant across ages in the Bossou chimpanzees (Schofield et al., 2023), two old-aged individuals became notably peripheral in social networks constructed using data from the 2011 field season (Schofield et al., 2019) (Yo and Velu; the two individuals we identified as having the lowest attendance rates), indicating that they were more often seen arriving at the outdoor laboratory alone or travelling as a pair. In tandem with the profound reduction in population size at Bossou throughout our study period (Matsuzawa et al., 2004), changes in social structure may have disproportionately affected elderly chimpanzees, leading to a lower likelihood of visiting the outdoor laboratory alongside – or to regroup with – other community members. Further research is required to link our observed changes in nut cracking engagement to their underlying causes.

Through the collection of longitudinal behavioral data, we were able to evaluate whether at older ages, chimpanzees perform less streamlined tool-use behaviors. At Bossou, chimpanzees exhibit interindividual variation in nut cracking efficiency; however, within-individual efficiency is stable over the majority of each chimpanzee’s lifetime (Berdugo et al., 2025). To assess for aging effects, we therefore compared behavior in middle and later adulthood for each chimpanzee, permitting signals of aging to be identified using individually bespoke baselines of efficiency. Focal chimpanzees exhibited high efficiency in the first field season (1999), suggesting that we began sampling data before the onset of tool-use senescence (see Biro et al., 2003 for data on striking efficiency of adults at Bossou, where all adults use approximately 2–4 strikes per oil-palm nut – our focal subset of adults fell within this range in 1999). Of the five individuals included in our study, three individuals took longer to select stone tools over progressing field seasons (Yo, Fana, and Jire), two females showed very small increases in the amount of time taken to crack and process nuts (Fana and Jire), whereas two other females exhibited comparatively dramatic increases in the time taken to crack and process each nut (Yo and Velu). Yo and Velu also exhibited more frequent striking using the hammer stone, and Yo performed additional actions to peel shell away from kernels with her mouth and consumed kernels with a greater number of bites (see Video 1 for footage of Yo cracking oil-palm nuts in 1999 and 2016). Our results therefore suggest that there is measurable interindividual variation in the effects of extreme aging on the efficiency of both tool selection and use in wild chimpanzees.

Video 1

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Our findings mirror reports of interindividual variability in the senescence of cognitive and physiological systems in both captive and wild primates (Tarou et al., 2002; Rothwell et al., 2021; Morbeck et al., 2002; Freire-Cobo et al., 2021; Hämäläinen et al., 2015). Whilst it is outside the scope of our study to determine the precise cognitive, physical, and resultant motivational changes that led to reductions in engagement with tools, rates of tool selection, and the efficiency of tool use, our results can generate predictions about how changes in fine-scale processes may translate into the behavioral changes we have observed with progressive aging. For the chimpanzees that experienced reductions in nut cracking efficiency (as discussed above), these changes could be due to changes in physical strength and dexterity (Lowenstine et al., 2016; Morbeck et al., 2002), visual acuity (Fujisawa et al., 2010), dentition (where tooth decay may render peeling and chewing actions more difficult; Lowenstine et al., 2016; Albrecht et al., 2024), or possibly due to changes in cognition relevant to effective tool use (Lacreuse et al., 2014; Lacreuse et al., 2020), such as executive functioning or working memory. Changes in tool use behavior may also have emerged to actively compensate for the effects of senescence that are not in themselves specific to tool use; for example, tooth wear and subsequent periodontal disease are common in old-aged chimpanzees (Lowenstine et al., 2016; Albrecht et al., 2024). The additional strikes of the hammer stone performed by Yo and Velu to crack oil-palm nuts may have therefore been motivated by the desire to break the kernel into a greater number of smaller pieces, which were easier to peel and consume. This conclusion is somewhat supported by post-mortem data for Velu following her death in 2017, as she exhibited heavy wear patterns on both incisors and premolars and was missing several molars on the lower jaw (Matsuzawa, 2018). Similarly to tool-using efficiency, the duration of tool selection may have taken longer for several individuals due to difficulties identifying the properties of available stones, perhaps due to changes in perceptual systems (such as poorer vision; Fujisawa et al., 2010), or cognitive challenges in predicting the properties of objects. Alternatively, longer tool-selection times could have also been due to the need for chimpanzees to weigh up the benefits of specific tool properties (e.g. weight and size), relative to age-related changes in their physical strength and mobility. Bridging the gap between age-related changes in tool-use behavior and changes in cognitive and physiological processes requires further study and would likely benefit from experimental approaches where possible.

Our study used longitudinal video data collected from a unique, decades-long systematic study of wild chimpanzee tool use, and this video archive likely represents the only currently available data source to study intraindividual variation in chimpanzee nut cracking across the span of decades (Berdugo et al., 2025). Moreover, given the exceptionally long lives of several chimpanzees at Bossou (Emery Thompson et al., 2007), Bossou represents a unique population whose individuals can be readily studied to examine the effects of senescence in the wild at the level of the individual. However, the use of existing video data and time-intensive methods for fine-scaled behavior coding means that our study faced a number of limitations.

Firstly, we were unable to analyze whether specific ecological variables – such as the availability of different food sources and demographic changes at Bossou – influence aging individuals’ attendance at the outdoor laboratory, as well as at naturally occurring nut cracking sites (see discussion above). Nevertheless, by using the attendance of younger individuals as a control, we were able to identify that the reduction in attendance over field seasons was limited to older individuals, suggesting a specific change in behavior associated with chimpanzees experiencing progressively old age. Further research is needed to understand what factors lead to this reduced engagement with nut cracking at older ages; how aging individuals compensate for calorie loss from reduced nut cracking, and more generally, how aging influences chimpanzees’ foraging behaviors across their entire home range.

Secondly, we were not able to eliminate all possible ecological explanations for age-related changes in tool-using efficiency (Falótico et al., 2022; Proffitt et al., 2022). Some ecological variables were controlled for as part of the experimental set up at the outdoor laboratory. For example, chimpanzees were always tested during similar months of the year in each field season, and were provided with oil-palm nuts at a suitable stage of maturity (and thus of similar hardness). Previous studies at Bossou have also revealed that chimpanzees are able to select nuts that are suitable for cracking, further suggesting that chimpanzees can account for differences in nut quality during tool use (Sakura and Matsuzawa, 1991; although this could also have been affected by aging itself, such as through reduced visual acuity impeding suitable nut selection; Fujisawa et al., 2010). Whilst it is possible that other ecological factors may influence our results, we believe that inter-seasonal ecological differences are unlikely to fully explain them. Firstly, if differences in chimpanzees’ nut cracking efficiency between seasons were being driven by ecological variation, we predict that this inter-annual variation would be equally present across early and late field seasons. However, contrary to this prediction, nut-cracking efficiency was very similar across early field seasons (and across individuals during these years); changes in efficiency were only detected in later field seasons, when chimpanzees were sampled at older ages. Secondly, if inter-annual differences in ecology rendered nut cracking more difficult in later field seasons, we would expect these ecological changes to affect all individuals similarly. This was also not the case, as changes in behavior differed between individuals – some maintained similar levels of efficiency (such as Fana), whereas other individuals experienced profound reductions in efficiency (such as Velu and Yo). For Yo (the individual with the greatest reduction in tool-using efficiency), the observations that Yo took even longer to crack oil-palm nuts in 2018 (and that Yo also struggled to crack coula nuts in 2011, see Appendices 3 and 4 for further information, and Video 2) provide evidence for a directional, individual-specific reduction in nut-cracking efficiency across later years, rather than her efficiency being dictated by ecological variation. We could not provide nut-cracking efficiency data for a cohort of younger adults across field seasons, as there was only one young adult (male) individual at Bossou between 1999 and 2016. An additional younger adult cohort would have been a desirable control group for our study, to complement the long-term efficiency baselines we provide at the level of the individual. For future studies, we believe that the collection of a wider array of ecological data would be valuable for discriminating between explanations with greater confidence and, where possible, future studies should aim to collect long-term data on the behavior of younger adults as additional control groups.

Video 2

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Thirdly, as data were collected from video footage, we could not examine how the dimensions of tools and raw material types influenced chimpanzees’ tool-use behaviors over different encounters and across field seasons. Throughout long-term data collection at Bossou, the stone tools available at the outdoor laboratory have been kept as consistent as possible, and chimpanzees select tools with physical properties which likely enhance nut cracking efficiency (Carvalho et al., 2008; Braun et al., 2025). Indeed, changes in tool-using efficiency may be borne from increasing difficulty selecting appropriate tools with aging. Future studies should gather data on tool properties to support analyses of aging effects in tool use. These studies could be combined with data collection on even more finely grained behaviors of apes when using tools, such as the specific grips used to manipulate objects over time (Neufuss et al., 2017; Malherbe et al., 2024).

Fourthly, our study was limited to a small sample size of five aging chimpanzees. This is an inevitability of collecting longitudinal data on long-lived wild individuals who are approaching the ends of their lifespan. Further data is needed – including from other field sites – to establish whether the variation in aging effects we have found generalizes to other individuals and populations (and, where possible, other tool use behaviors).

Much like human technical skills, the tool-use behaviors of chimpanzees and other great apes are culturally variable behaviors that are acquired through a mixture of social learning and individual practice (Matsuzawa et al., 2011; Inoue-Nakamura and Matsuzawa, 1997; Biro et al., 2003; Schuppli et al., 2016). As previously mentioned, prior research on nut cracking behavior at Bossou has revealed that chimpanzees vary in the age of skill acquisition (Matsuzawa et al., 2011; Inoue-Nakamura and Matsuzawa, 1997), and the efficiency with which nut cracking is performed across adulthood varies between individuals, yet is stable within individuals over time (Berdugo et al., 2025). These differences in individual performance are, in part, likely due to differences in the environments of learners during skill acquisition (Berdugo et al., 2024). Our results expand on these findings to highlight that, whilst chimpanzees at Bossou perform nut cracking behaviors throughout their lives (suggesting that this is an important skill for this population), progressive aging and senescence may exaggerate interindividual differences in the performance of socially learnt skills, as seen in humans (Lindenberger, 2014; Paccagnella, 2016). Taken as a whole, our results provide further evidence that the cultural behaviors of humans and chimpanzees exhibit marked similarities that extend across their lifetimes, including, for some individuals, a period of technological senescence that can manifest across the oldest years of life. Further research should examine whether similar factors influence senescence of technical skills between humans and apes. This research should include studies that determine whether skill proficiency in early life and adulthood, and the frequency with which skills continue to be performed in later life, influence the rate and likelihood of senescence. Furthermore, debate continues as to whether human behaviors are particularly susceptible to the effects of aging due to the development of neurodegenerative diseases, such as Alzheimer’s and Parkinson’s disease (Edler et al., 2021; Finch and Austad, 2015; Blesa et al., 2018; Emborg, 2017). Current evidence suggests that the effects of these neurological changes in humans have far more profound impacts on behavior, despite primates sometimes exhibiting similar neuropathological signatures during aging (Frye et al., 2022; Arnsten et al., 2019; Edler et al., 2017; Lemere et al., 2008). Yet, it is still not clear whether this conclusion comes from a lack of behavioral data on aging in primates. We were not able to collect neurological samples from the chimpanzees in our study and cannot say whether the changes we observed could be associated with such processes (including for Yo, whose more profound senescence renders her the most likely to suffer from neurological decline). However, tool use could offer a suitable domain in which to examine the possible manifestation of such diseases (if present). Field sites should make specific efforts to collect long-term data on behavioral changes with aging – including for tool use – and where possible aim to sample neurological data following the natural deaths of wild, elderly individuals. These data will provide important insights into the underlying causes of human and chimpanzee skill disruption in the contexts of healthy and diseased aging.

In foraging contexts, multi-object tool-use behaviors are often used to extract energy-rich resources that would not be otherwise accessible (King, 1986). Given the sample size of our study and limitations in the wider ecological data available, it was not possible to identify the influence of tool-use senescence on individual survivability through reduced energy intake. Answering this question would require data on a greater number of tool-use behaviors, spanning across the home range. However, the two females in our study who exhibited limited changes in tool-using efficiency (Jire and Fana) had the longest lifespan after the end of our study, whereas Velu and Yo (who experienced greater difficulty cracking nuts in later years) died comparatively shortly after our sample period. While this sample is too small to make strong claims, this pattern could indicate that the senescence of tool-use behaviors, and the energy-rich foods to which they permit access, can contribute to reduced survivability in the wild. Alternatively, changes in tool-use behaviors could offer a litmus for identifying individuals experiencing profound generalized senescence in the wild, where changes in many physiological and behavioral processes subsequently impact an individual’s survivability. By extension, outside of tool use, our data on individual survivability – alongside previous studies of chimpanzees at Bossou – invites speculation surrounding whether the social relationships of specific individuals may reduce or accentuate the rate and intensity of senescence with progressive aging. In addition to living for a longer period after the final field season we sampled, Fana and Jire enjoyed more central social positions than other elderly females at Bossou (Schofield et al., 2019) and had a greater number of living relatives during the latter field seasons (during which Jire had two mature offspring, and Fana had two mature offspring and two young grandchildren). Given that only eight individuals remained at Bossou by 2016, these familial relationships constituted a significant proportion of the overall community. Further research will provide insight into if and how lifetime sociality and familial success influence the onset and rate of senescence in wild chimpanzees, for example through socially mediated resource acquisition.

In sum, we demonstrate that the tool-use behaviors of wild chimpanzees can change in old age, and that these changes vary between individuals. Whilst our study is observational, we argue that processes of senescence offer a promising explanation for such changes, particularly in regard to changes in individual tool-using efficiency. Our findings reflect the conclusions of previous studies investigating the cognitive and physiological senescence of primates living in captivity and generate a myriad of further questions about the possible underlying mechanisms of tool-use senescence, as well as more general behavioral aging in wild apes. As questions surrounding aging benefit from longitudinal data – which for many primates require collection across decades – the possibility that such questions will be answered is becoming increasingly more precarious in an age where primates are at a heightened risk of extinction (Estrada et al., 2017). The conservation of wild primate populations is paramount for our understanding of the dynamics and evolution of primate aging processes, which may reveal insights into the forces influencing behavioral stability and senescence across the human lifetime.

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Author details

1. Elliot Howard-Spink

   1. Department of Biology, University of Oxford, Oxford, United Kingdom
   2. Development and Evolution of Cognition Group, Max Planck Institute of Animal Behavior, Konstanz, Germany
   3. School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing - original draft, Writing – review and editing

   For correspondence

   elliot.howardspink@outlook.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3961-3982

2. Tetsuro Matsuzawa

   1. Department of Pedagogy, Chubu Gakuin University, Gifu, Japan
   2. College of Life Science, Northwest University, Xi’an, China

   Contribution

   Resources, Data curation, Funding acquisition, Investigation, Methodology, Project administration, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-8147-2725

3. Susana Carvalho

   1. Department of Science, Gorongosa National Park, Sofala, Mozambique
   2. Interdisciplinary Center for Archaeology and Evolution of Human Behaviour (ICArEHB), Universidade do Algarve, Faro, Portugal
   3. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Vairão, Portugal

   Contribution

   Data curation, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4542-3720

4. Catherine Hobaiter

   Wild Minds Lab, School of Psychology and Neuroscience, University of St Andrews, St Andrews, United Kingdom

   Contribution

   Data curation, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3893-0524

5. Katarina Almeida-Warren

   1. Interdisciplinary Center for Archaeology and Evolution of Human Behaviour (ICArEHB), Universidade do Algarve, Faro, Portugal
   2. School of Anthropology and Museum Ethnography, University of Oxford, Oxford, United Kingdom

   Contribution

   Data curation, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7634-9466

6. Thibaud Gruber

   Faculty of Psychology and Educational Sciences, and Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland

   Contribution

   Conceptualization, Supervision, Methodology, Writing – review and editing, Cosenior Author

   Contributed equally with

   Dora Biro

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6766-3947

7. Dora Biro

   Department of Brain and Cognitive Sciences, University of Rochester, Rochester, United States

   Contribution

   Conceptualization, Data curation, Supervision, Investigation, Methodology, Writing – review and editing, Cosenior Author

   Contributed equally with

   Thibaud Gruber

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3408-6274

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