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

Reviewer #1 (Public review):

Summary:

Howard-Spink et al. investigated how older chimpanzees changed their behavior regarding stone tool use for nutcracking over a period of 17 years, from late adulthood to old age. This behavior is cognitively demanding, and it is a good target for understanding aging in wild primates. They used several factors to follow the aging process of five individuals, from attendance at the nut-cracking outdoor laboratory site to time to select tools and efficiency in nut-cracking to check if older chimpanzee changed their behavior.

Indeed, older chimpanzees reduced their visits to the outdoor lab, which was not observed in the younger adults. The authors discuss several reasons for that; the main ones being physiological changes, cognitive and physical constraints, and changes in social associations. Much of the discussion is hypothetical, but a good starting point, as there is not much information about senescence in wild chimpanzees.

The efficiency for nut-cracking was variable, with some individuals taking a long time to crack nuts while others showed little variance. As this is not compared with the younger individuals and the sample is small (only five individuals), it is difficult to be sure if this is also partly a normal variance caused by other factors (ecology) or is only related to senescence.

Strengths:

(1) 17 years of longitudinal data in the same setting, following the same individuals.

(2) Using stone tool use, a cognitively demanding behavior, to understand the aging process.

Weaknesses:

A lack of comparison of the stone tool use behavior with younger individuals in the same period, to check if the changes observed are only related to age or if it is an overall variance. The comparison with younger chimpanzees was only done for one of the variables (attendance).

Reviewer #2 (Public review):

Summary:

Primates are a particularly important and oft-applied model for understanding the evolution of, e.g., life history and senescence in humans. Although there is a growing body of work on aging in primates, there are three components of primate senescence research that have been underutilized or understudied: (1) longitudinal datasets, (2) wild populations, and (3) (stone) tool-use behaviors. Therefore, the goal of this study was to (1) use a 17-year longitudinal dataset (2) of wild chimpanzees in the Bossou forest, (3) visiting a site for field experiments on nut-cracking. They sampled and analyzed data from five field seasons for five chimpanzees of old age. From this sample, Howard-Spink and colleagues noted a decline in tool-use and tool-use efficiency in some individuals, but not in others. The authors then conclude that there is a measurable effect of senescence on chimpanzee behavior, but that it varies individually. The study has major intellectual value as a building block for future research, but there are several major caveats.

Strengths:

With this study, Howard-Spink and colleagues make a foray into a neglected topic of research: the impact of the physiological and cognitive changes due to senescence on stone tool use in chimpanzees. Based on novelty alone, this is a valuable study. The authors cleverly make use of a longitudinal record covering 17 years of field data, which provides a window into long-term changes in the behavior of wild chimpanzees, which I agree cannot be understood through cross-sectional comparisons.

The metrics of 'efficiency' (see caveats below) are suitable for measuring changes in technological behavior over time, as specifically tailored to the nut-cracking (e.g., time, number of actions, number of strikes, tool changes). The ethogram and the coding protocol are also suitable for studying the target questions and objectives. I would recommend, however, the inclusion of further variables that will assist in improving the amount of valid data that can be extrapolated (see also below).

With this pilot, Howard-Spink and colleagues have established a foundation upon which future research can be designed, including further investigation with the Bossou dataset and other existing video archives, but especially future targeted data collection, which can be designed to overcome some of the limits and confounds that can be identified in the current study.

Weaknesses:

Although I agree with the reasoning behind conducting this research and understand that, as the authors state, there are logistical considerations that have to be made when planning and executing such a study, there are a number of methodological and theoretical shortcomings that either need to be more explicitly stated by the authors or would require additional data collection and analysis.

One of the main limitations of this study is the small sample size. There are only 5 of the old-aged individuals, which is not enough to draw any inferences about aging for chimpanzees more generally. Howard-Spink and colleagues also study data from only five of the 17 years of recorded data at Bossou. The selection of this subset of data requires clarification: why were these intervals chosen, why this number of data points, and how do we know that it provides a representative picture of the age-related changes of the full 17 years?

With measuring and interpreting the 'efficiency' of behaviors, there are in-built assumptions about the goals of the agents and how we can define efficiency. First, it may be that efficiency is not an intentional goal for nut-cracking at all, but rather, e.g., productivity as far as the number of uncrushed kernels (cf. Putt 2015). Second, what is 'efficient' for the human observer might not be efficient for the chimpanzee who is performing the behavior. More instances of tool-switching may be considered inefficient, but it might also be a valid strategy for extracting more from the nuts, etc. Understanding the goals of chimpanzees may be a difficult proposition, but these are uncertainties that must be kept in mind when interpreting and discussing 'decline' or any change in technological behaviors over time.

For the study of the physiological impact of senescence of tool use (i.e., on strength and coordination), the study would benefit from the inclusion of variables like grip type and (approximate) stone size (Neufuss et al., 2016). The size and shape of stones for nut-cracking have been shown to influence the efficacy and 'efficiency' of tool use (i.e., the same metrics of 'efficiency' implemented by Howard-Spink et al. in the current study), meaning raw material properties are a potential confound that the authors have not evaluated.

Similarly, inter- and intraspecific variation in the properties of nuts being processed is another confound (Falótico et al., 2022; Proffitt et al., 2022). If oil palm nuts were varying year-to-year, for example, this would theoretically have an effect on the behavioral forms and strategies employed by the chimpanzees, and thus, any metric of efficiency being collected and analyzed. Further, it is perplexing that the authors analyze only one year where the coula nuts were provided at the test site, but these were provided during multiple field seasons. It would be more useful to compare data from a similar number of field seasons with both species if we are to study age-related changes in nut processing over time (one season of coula nut-cracking certainly does not achieve this).

Both individual personality (especially neophilia versus neophobia; e.g., Forss & Willems, 2022) and motivation factors (Tennie & Call, 2023) are further confounds that can contribute to a more valid interpretation of the patterns found. To draw any conclusions about age-related changes in diet and food preferences, we would need to have data on the overall food intake/preferences of the individuals and the food availability in the home range. The authors refer briefly to this limitation, but the implications for the interpretation of the data are not sufficiently underlined (e.g., for the relevance of age-related decline in stone tool-use ability for individual survival).

Generally speaking, there is a lack of consideration for temporal variation in ecological factors. As a control for these, Howard-Spink and colleagues have examined behavioral data for younger individuals from Bossou in the same years, to ostensibly show that patterns in older adults are different from patterns in younger adults, which is fair given the available data. Nonetheless, they seem to focus mostly on the start and end points and not patterns that occur in between. For example, there is a curious drop in attendance rate for all individuals in the 2008 season, the implications of which are not discussed by the authors.

As far as attendance, Howard-Spink and colleagues also discuss how this might be explained by changes in social standing in later life (i.e., chimpanzees move to the fringes of the social network and become less likely to visit gathering sites). This is not senescence in the sense of physiological and cognitive decline with older age. Instead, the reduced attendance due to changes in social standing seems rather to exacerbate signs of aging rather than be an indicator of it itself. The authors also mention a flu-like epidemic that caused the death of 5 individuals; the subsequent population decline and related changes in demography also warrant more discussion and characterization in the manuscript.

Understandably, some of these issues cannot be evaluated or corrected with the presented dataset. Nonetheless, these undermine how certain and/or deterministic their conclusions can really be considered. Howard-Spink et al. have not strongly 'demonstrated' the validity of relationships between the variables of the study. If anything, their cursory observations provide us with methods to apply and hypotheses to test in future studies. It is likely that with higher-resolution datasets, the individual variability in age-related decline in tool-use abilities will be replicated. For now, this can be considered a starting point, which will hopefully inspire future attempts to research these questions.

Falótico, T., Valença, T., Verderane, M. & Fogaça, M. D. Stone tools differences across three capuchin monkey populations: food's physical properties, ecology, and culture. Sci. Rep. 12, 14365 (2022).
Forss, S. & Willems, E. The curious case of great ape curiosity and how it is shaped by sociality. Ethology 128, 552-563 (2022).
Neufuss, J., Humle, T., Cremaschi, A. & Kivell, T. L. Nut-cracking behaviour in wild-born, rehabilitated bonobos (Pan paniscus): a comprehensive study of hand-preference, hand grips and efficiency. Am. J. Primatol. 79, e22589 (2016).
Proffitt, T., Reeves, J. S., Pacome, S. S. & Luncz, L. V. Identifying functional and regional differences in chimpanzee stone tool technology. R. Soc. Open Sci. 9, 220826 (2022).
Putt, S. S. The origins of stone tool reduction and the transition to knapping: An experimental approach. J. Archaeol. Sci.: Rep. 2, 51-60 (2015).
Tennie, C. & Call, J. Unmotivated subjects cannot provide interpretable data and tasks with sensitive learning periods require appropriately aged subjects: A Commentary on Koops et al. (2022) "Field experiments find no evidence that chimpanzee nut cracking can be independently innovated". ABC 10, 89-94 (2023).

Author response:

We thank both reviewers for their comments on our manuscript. We are pleased that the value of this research has been communicated effectively, and that the reviewers agree that whilst our sample size of individuals is relatively small, it offers a unique perspective for understanding the effects of aging for wild chimpanzees’ technological behaviors. Whilst only yielding data on a few individuals, the Bossou archive is the only available data source with which we can currently address these questions over extended timescales, and is key for understanding longitudinal effects of aging for specific individuals. This is particularly true if we are to understand the life-long dynamics of chimpanzees’ technical skills during tasks which require the organization of multiple movable elements. Bossou is the only community where chimpanzees both perform nut cracking with moveable hammer and anvil stones, and have been systematically studied over a period of decades. Moreover, given the dwindling population at Bossou (N = 3 as of 2025), we must make every effort to understand these effects with existing data. We agree that this work will likely form a valuable foundation for future studies, which may aim to either replicate our results, or use our findings to design more specific research questions and approaches.

In the next iteration of the manuscript, we will elaborate on our choice of field seasons more clearly. However, this was a logistical tradeoff between needing to sample across a long lifespan using fine-granularity behavior coding, versus the time constraints for our project and the likely yield of data collection. We sampled from the middle of individuals’ prime age, up until the oldest recorded ages of individuals lifespans (17 years). Where possible we aimed to use consistent time intervals (approximately 4 years); however, this was not always possible, as in some years data was not collected by researchers at Bossou (for example, during years where there were Ebola outbreaks affecting the region). In such instances, we sampled the closest available year that offered sufficient data to meet our sampling requirements).

Reviewer 2 raises that there may be a disconnect between how human observers and chimpanzees conceive of efficiency when nut cracking, and support this idea with a citation to previous work on efficiency of Oldowan stone knapping. We agree that knowing precisely how chimpanzees perceive their own efficiency during tool use is not available through observation alone, nor can we assess the true extent to which chimpanzees are concerned about the efficiency of their nut-cracking. However, following previous studies, it is reasonable to assume that adult chimpanzees embody some level of efficiency, given that adults often select tools which aid efficient nut cracking (Braun et al. 2025, J. Hum. Evol.; Carvalho et al. 2008, J. Hum. Evol.; Sirianni et al. 2015, Animal Behav.); perform nut cracking using more streamlined combinations of actions than less experienced individuals (Howard-Spink et al. 2024, Peer J; Inoue-Nakamura & Matsuzawa 1997, J. Comp. Psychol.), and consequently end up cracking nuts using fewer hammer strikes, indicating a higher level of skill (Biro et al. 2003, Animal Cogn.; Boesch et al. 2019, Sci. Rep.). Ultimately, these factors suggest that across adulthood, experienced chimpanzees perform nut cracking with a level of efficiency which exceeds novice individuals, including across the chaine operatoire.

To account for the multiple ways in which reduced efficiency may manifest later in life, we provide one of the most flexible measures of efficiency in wild chimpanzee tool use to date, which incorporates more classical measures of time and hammer strikes (see previous examples of Biro et al. 2003, Animal Cogn.; Boesch et al. 2019 Sci. Rep.) as well as additional variables which aim to characterize how streamlined behavioral sequences are (tool rotations, tool swaps, nut replacements, etc. see Berdugo et al. 2024 Nat. Hum. Behav for other analyses using similar metrics). In the case of swapping out tools, Reviewer 2 suggests that some of these tool swaps may in fact be to aid nut cracking, by maintaining kernel integrity (a key result relating to Yo’s coula nut cracking efficiency). This however seems unlikely, given that these behaviors were performed extremely rarely by chimpanzees in early field seasons, and were not performed more frequently by other individuals with aging. We will provide additional information behind our metrics for measuring efficiency, with reference to earlier work, and also will incorporate the points raised by Reviewer 2 concerning the limitations with which we can infer chimpanzees’ goals, and how efficiently they meet them.

Reviewer 1 questioned why we did not sample efficiency data for younger individuals, and compare this data with older individuals to detect the effects of aging. Throughout our manuscript, we compared aging individuals’ nut-cracking efficiency with their efficiency in previous years (thus, at younger ages). This offered each individual personalized benchmark of efficiency in early life, and allowed us to identify aging effects whilst controlling for long-term interindividual variation in skill levels. Indeed, previous analyses at Bossou find that across the majority of adulthood, efficiency varies between individuals, but is relatively stable within individuals (see Berdugo et al. 2024, Nat. Hum. Behav.). As focal aging chimpanzees cracked multiple nuts each field season (and each encounter), we had ample data to fit models that examine individuals’ efficiency over field seasons, using random slopes to model correlations for each individual. By taking this approach, our paper offers a novel perspective by being able to report the longitudinal effects of aging on tool-using efficiency, rather than averaged cross-sectional effects between young and old cohorts. As random slope models (and not just random intercept models) offered the best explanation for variation in aging individuals’ efficiency over our sample period, this implies that focal chimpanzees were experiencing individual-level changes in efficiency over time, thus giving us key evidence that interindividual variation in tool-using efficiency can be compounded by aging.

We argue that the reductions in efficiency observed for some individuals (e.g. Yo & Velu) are unlikely to be due to environmental changes (e.g. nuts becoming harder in later field seasons), as if this was the case, these effects would be detected across the behaviors of all individuals (which was not observed). Additionally, in the specific case of the hardness of nuts, nuts used in our experiment were sourced from local communities, and were moderately aged. This avoided the use of young nuts which are harder to crack, or older nuts which are often worm-eaten or can be empty (Sakura & Matsuzawa, 1991; Ethology). We will update our manuscript with this information.

Whilst other factors may introduce general variation into our efficiency data (such as different stones used on different encounters, or more general variation in nut hardness across encounters), very few of these factors predict directional long-term changes in efficiency. Rather, if these factors were driving the majority of variation in our data, we would expect them to lead to variation across visits during earlier field seasons (such as 1999-2008) and later field seasons (2011 onwards) equally, and in a way which does not necessarily correlate with age. This does not match the pattern we observed in our data, where for some individuals (e.g. Yo & Velu), efficiency in nut cracking reduced in later field seasons only, and was relatively consistent across field seasons prior to 2011. Moreover, for Yo – the individual who exhibited the greatest reductions in tool-using efficiency - efficiency continued to decrease across the three of the latest sampled field seasons. Thus, it is more likely Yo was experiencing deleterious effects of aging. We do however agree that additional data on these variables would help us to remove the possibility of compounding factors more rigorously – we will include recommendations for this data to be collected in future studies.

When modelling the effect of aging on attendance at the outdoor laboratory, we could not use the same approach we used when modelling tool-using efficiency, as we could only acquire one datapoint (attendance rate) per individual for each field season. We therefore had to adapt our analysis, and introduce attendance rates for younger individuals as a baseline to compare against the attendance rates of older individuals across years. We observed a significant interaction effect, where across field seasons, attendance dropped significantly more rapidly for older individuals than younger ones. Reviewer 2 has asked why we do not consider inter-annual variability across this time period, and suggested that we ignored intervening years. This is not the case. When fitting models that examined the effects of aging on attendance, we used all data across all field seasons. We reported an approximate effect size for this significant correlation using a digestible comparison of the attendance rates in the initial and final field seasons sampled. We will ensure that this is clear in the next iteration of our manuscript.

Reviewer 2 noted that many factors may have influenced the decision for chimpanzees to attend the outdoor laboratory in older field seasons, and the current data may not be used to make strong arguments for changes in attendance rates being due to dietary preferences. We agree that many factors may have influenced these attendance rates, and that is what we have aimed to transparently report within our discussion where we raise an extensive, non-exhaustive list of hypotheses for why we have observed this age-related change in our data. We will aim to ensure that this is exceptionally clear prior to resubmission, and where relevant, will further emphasize points raised by Reviewer 2. We consider some points raised by Reviewer 2 to be unlikely to apply for our study; for example, it is unlikely neophobia has influenced the behaviors of chimpanzees, as these chimpanzees habitually attended the outdoor laboratory at their own accord for over a decade prior to the earliest year we sampled in this study (reflecting extremely high levels of habituation to the experimental set up). Previous studies at Bossou have surveyed the ecology of stone tool use across the home range, and confirm that the outdoor laboratory is visited by chimpanzees during ranging as a food patch (Almeida-Warren et al. 2022 Int. J. Primatol.).

Reviewer 2 suggested that it would be helpful to have additional data on variables such as hand grip, as this may reveal further information about how cognitive and physiological senescence influences reductions in tool-using efficiency. We agree that whilst further data on hand grips are not required to detect reductions in efficiency per say per se, it would be profitable for future analyses to collect similar data – we will add this as a recommendation to our discussion.

Finally, Reviewer 2 commented that they found our discussion of coula-nut cracking disruptive to the flow of the manuscript, given that we could not compare with coula-nut cracking in earlier years. We reported the coula nut cracking of Yo in 2011 as it was part of our sampled data, and we felt that the comparison with other individuals in the same year was an interesting discussion point, however we acknowledge this limitation. We will move all data and discussion of coula-nut cracking to the Supplementary Materials, which we will present as an interesting additional observation which may warrant further investigation using additional data from the Bossou archive. Data collection for this future project could include collecting data on the additional variables raised by both reviewers (e.g. hand grips).

We thank both reviewers for their comments. We believe that their feedback will improve the quality of our reporting, and the validity of our interpretations.