Urbanization does not increase "object curiosity" in vervet monkeys, but semi-urban individuals selectively explore food-related anthropogenic items.

Urban environments expose animals to abundant anthropogenic materials and foods that facilitate foraging innovations in species with opportunistic diets and high behavioral flexibility. Neophilia and exploration tendency are believed to be important behavioral traits for animals thriving in urban environments. Vervet monkeys (Chlorocebus pygerythrus) are one of few primate species that have successfully adapted to urban environments, thus making them an ideal species to study these traits. Using a within-species cross-habitat approach, we compared neophilia and exploration of novel objects (jointly referred to as "object curiosity") between semi-urban, wild, and captive monkeys to shed light on the cognitive traits facilitating urban living. To measure "object curiosity," we exposed monkeys to various types of novel stimuli and compared their approaches and explorative behavior. Our results revealed differences in the number of approaches and explorative behavior toward novel stimuli between the habitat types considered. Captive vervet monkeys were significantly more explorative than both semi- urban and wild troops, suggesting that positive experiences with humans and lack of predation, rather than exposure to human materials per se, influence object curiosity. Across habitats, juvenile males were the most explorative age-sex class. This is likely due to males being the dispersing sex and juveniles being more motivated to learn about their environment. Additionally, we found that items potentially associated with human food, elicited stronger explorative responses in semi-urban monkeys than non-food related objects, suggesting that their motivation to explore might be driven by "anthrophilia", that is, their experience of rewarding foraging on similar anthropogenic food sources. We conclude that varying levels of exposure to humans, predation and pre-exposure to human food packaging explain variation in "object curiosity" in our sample of vervet monkeys.

Social responses to a hurricane drive greater epidemic risk.

The increasing frequency and intensity of extreme weather events due to climate change has the potential to alter ecosystem dynamics and wildlife health. Here we show that increasing social connections in response to a hurricane enhanced disease transmission risk for years after the event in a population of rhesus macaques. Our findings reveal that behavioural responses to natural disasters can elevate epidemic risk, thereby threatening wildlife health, population viability, and spillover to humans.

Bone-related behaviours of captive chimpanzees (Pan troglodytes) during two excavating experiments.

After stone tools, bone tools are the most abundant artefact type in the Early Pleistocene archaeological record. That said, they are still relatively scarce, which limits our understanding of the behaviours that led to their production and use. Observations of extant primates constitute a unique source of behavioural data with which to construct hypotheses about the technological forms and repertoires exhibited by our hominin ancestors. We conducted two different experiments to investigate the behavioural responses of two groups of captive chimpanzees (Pan troglodytes; n = 33 and n = 9) to disarticulated, defleshed, ungulate bones while participating in a foraging task aimed at eliciting excavating behaviour. Each chimpanzee group was provided with bone specimens with different characteristics, and the two groups differed in their respective experience levels with excavating plant tools. We found that several individuals from the inexperienced group used the provided bones as tools during the task. In contrast, none of the individuals from the experienced group used bones as excavating tools, but instead continued using plant tools. These chimpanzees also performed non-excavating bone behaviours such as percussion and tool-assisted extraction of organic material from the medullary cavity. Our findings serve as a proof-of-concept that chimpanzees can be used to investigate spontaneous bone tool behaviours such as bone-assisted excavation. Furthermore, our results raise interesting questions regarding the role that bone characteristics, as well as previous tool-assisted excavating experience with other raw materials, might have in the expression of bone tool-assisted excavation.

Experimental investigation of orangutans' lithic percussive and sharp stone tool behaviours.

Early stone tools, and in particular sharp stone tools, arguably represent one of the most important technological milestones in human evolution. The production and use of sharp stone tools significantly widened the ecological niche of our ancestors, allowing them to exploit novel food resources. However, despite their importance, it is still unclear how these early lithic technologies emerged and which behaviours served as stepping-stones for the development of systematic lithic production in our lineage. One approach to answer this question is to collect comparative data on the stone tool making and using abilities of our closest living relatives, the great apes, to reconstruct the potential stone-related behaviours of early hominins. To this end, we tested both the individual and the social learning abilities of five orangutans to make and use stone tools. Although the orangutans did not make sharp stone tools initially, three individuals spontaneously engaged in lithic percussion, and sharp stone pieces were produced under later experimental conditions. Furthermore, when provided with a human-made sharp stone, one orangutan spontaneously used it as a cutting tool. Contrary to previous experiments, social demonstrations did not considerably improve the stone tool making and using abilities of orangutans. Our study is the first to systematically investigate the stone tool making and using abilities of untrained, unenculturated orangutans showing that two proposed pre-requisites for the emergence of early lithic technologies-lithic percussion and the recognition of sharp-edged stones as cutting tools-are present in this species. We discuss the implications that ours and previous great ape stone tool experiments have for understanding the initial stages of lithic technologies in our lineage.

Captivity and habituation to humans raise curiosity in vervet monkeys.

The cognitive mechanisms causing intraspecific behavioural differences between wild and captive animals remain poorly understood. Although diminished neophobia, resulting from a safer environment and more "free" time, has been proposed to underlie these differences among settings, less is known about how captivity influences exploration tendency. Here, we refer to the combination of reduced neophobia and increased interest in exploring novelty as "curiosity", which we systematically compared across seven groups of captive and wild vervet monkeys (Chlorocebus pygerythrus) by exposing them to a test battery of eight novel stimuli. In the wild sample, we included both monkeys habituated to human presence and unhabituated individuals filmed using motion-triggered cameras. Results revealed clear differences in number of approaches to novel stimuli among captive, wild-habituated and wild-unhabituated monkeys. As foraging pressure and predation risks are assumed to be equal for all wild monkeys, our results do not support a relationship between curiosity and safety or free time. Instead, we propose "the habituation hypothesis" as an explanation of why well-habituated and captive monkeys both approached and explored novelty more than unhabituated individuals. We conclude that varying levels of human and/or human artefact habituation, rather than the risks present in natural environments, better explain variation in curiosity in our sample of vervet monkeys.

Captive great apes tend to innovate simple tool behaviors quickly.

Recent studies have highlighted the important role that individual learning mechanisms and different forms of enhancenment play in the acquisition of novel behaviors by naïve individuals. A considerable subset of these studies has focused on tool innovation by our closest living relatives, the great apes, to better undestand the evolution of technology in our own lineage. To be able to isolate the role that individual learning plays in great ape tool innovation, researchers usually employ what are known as baseline tests. Although these baselines are commonly used in behavioral studies in captivity, the length of these tests in terms of number of trials and duration remains unstandarized across studies. To address this methodological issue, we conducted a literature review of great ape tool innovation studies conducted in zoological institutions and compiled various methodological data including the timing of innovation. Our literature review revealed an early innovation tendency in great apes, which was particularly pronounced when simple forms of tool use were investigated. In the majority of experiments where tool innovation took place, this occurred within the first trial and/or the first hour of testing. We discuss different possible sources of variation in the latency to innovate such as testing setup, species and task. We hope that our literature review helps researchers design more data-informed, resource-efficient experiments on tool innovation in our closest living relatives.

Evaluating the influence of action- and subject-specific factors on chimpanzee action copying.

The ability to imitate has been deemed crucial for the emergence of human culture. Although non-human animals also possess culture, the acquisition mechanisms underlying behavioural variation between populations in other species is still under debate. It is especially controversial whether great apes can spontaneously imitate. Action- and subject-specific factors have been suggested to influence the likelihood of an action to be imitated. However, few studies have jointly tested these hypotheses. Just one study to date has reported spontaneous imitation in chimpanzees (Persson et al. 2017 Primates 59, 19-29), although important methodological limitations were not accounted for. Here, we present a study in which we (i) replicate the above-mentioned study addressing their limitations in an observational study of human-chimpanzee imitation; and (ii) aim to test the influence of action- and subject-specific factors on action copying in chimpanzees by providing human demonstrations of multiple actions to chimpanzees of varying rearing background. To properly address our second aim, we conducted a preparatory power analysis using simulated data. Contrary to Persson et al.'s study, we found extremely low rates of spontaneous chimpanzee imitation and we did not find enough cases of action matching to be able to apply our planned model with sufficient statistical power. We discuss possible factors explaining the lack of observed action matching in our experiments compared with previous studies.

The Method of Local Restriction: in search of potential great ape culture-dependent forms.

Humans possess a perhaps unique type of culture among primates called cumulative culture. In this type of culture, behavioural forms cumulate changes over time, which increases their complexity and/or efficiency, eventually making these forms culture-dependent. As changes cumulate, culture-dependent forms become causally opaque, preventing the overall behavioural form from being acquired by individuals on their own; in other words, culture-dependent forms must be copied between individuals and across generations. Despite the importance of cumulative culture for understanding the evolutionary history of our species, how and when cumulative culture evolved is still debated. One of the challenges faced when addressing these questions is how to identify culture-dependent forms that result from cumulative cultural evolution. Here we propose a novel method to identify the most likely cases of culture-dependent forms. The 'Method of Local Restriction' is based on the premise that as culture-dependent forms are repeatedly transmitted via copying, these forms will unavoidably cumulate population-specific changes (due to copying error) and therefore must be expected to become locally restricted over time. When we applied this method to our closest living relatives, the great apes, we found that most known ape behavioural forms are not locally restricted (across domains and species) and thus are unlikely to be acquired via copying. Nevertheless, we found 25 locally restricted forms across species and domains, three of which appear to be locally unique (having been observed in a single population of a single species). Locally unique forms represent the best current candidates for culture-dependent forms in non-human great apes. Besides these rare exceptions, our results show that overall, ape cultures do not rely heavily on copying, as most ape behaviours appear across sites and/or species, rendering them unlikely to be culture-dependent forms resulting from cumulative cultural evolution. Yet, the locally restricted forms (and especially the three locally unique forms) identified by our method should be tested further for their potential reliance on copying social learning mechanisms (and in turn, for their potential culture-dependence). Future studies could use the Method of Local Restriction to investigate the existence of culture-dependent forms in other animal species and in the hominin archaeological record to estimate how widespread copying is in the animal kingdom and to postulate a timeline for the emergence of copying in our lineage.

Naïve, unenculturated chimpanzees fail to make and use flaked stone tools.

Background: Despite substantial research on early hominin lithic technologies, the learning mechanisms underlying flake manufacture and use are contested. To draw phylogenetic inferences on the potential cognitive processes underlying the acquisition of both of these abilities in early hominins, we investigated if and how one of our closest living relatives, chimpanzees ( Pan troglodytes), could learn to make and use flakes. Methods: Across several experimental conditions, we tested eleven task-naïve chimpanzees (unenculturated n=8, unknown status n=3) from two independent populations for their abilities to spontaneously make and subsequently use flakes as well as to use flakes made by a human experimenter. Results: Despite the fact that the chimpanzees seemed to understand the requirements of the task, were sufficiently motivated and had ample opportunities to develop the target behaviours, none of the chimpanzees tested made or used flakes in any of the experimental conditions. Conclusions: These results differ from all previous ape flaking experiments, which found flake manufacture and use in bonobos and one orangutan. However, these earlier studies tested human-enculturated apes and provided test subjects with flake making and using demonstrations. The contrast between these earlier positive findings and our negative findings (despite using a much larger sample size) suggests that enculturation and/or demonstrations may be necessary for chimpanzees to acquire these abilities. The data obtained in this study are consistent with the hypothesis that flake manufacture and use might have evolved in the hominin lineage after the split between Homo and Pan 7 million years ago, a scenario further supported by the initial lack of flaked stone tools in the archaeological record after this split. We discuss possible evolutionary scenarios for flake manufacture and use in both non-hominin and hominin lineages.

Chimpanzees' (Pan troglodytes) problem-solving skills are influenced by housing facility and captive care duration.

Although a large body of primate cognition research is done in captive institutions, little is known about how much individuals from different facilities vary in their experiences and cognitive skills. Here we present the results of an experimental study investigating how physical cognitive skills vary between chimpanzees in relation to captive settings and their time in captivity. We tested 59 chimpanzees housed at two different captive facilities (a rehabilitation center (sanctuary) and a zoo) in three problem-solving tasks. Our results showed that chimpanzees at the two housing facilities significantly differed in overall task performance. On average, the sanctuary chimpanzees outperformed the chimpanzees housed at the zoo in the detour reaching task and the honey trap task. However, the zoo chimpanzees performed slightly better on average in the learning task. We propose that, for this particular sample, the documented differences result from a combination of factors, such as prior experience with cognitive testing, motivation levels and varying degrees of human exposure. Within the sanctuary sample, we found that chimpanzees who arrived at an earlier age at the sanctuary and had therefore spent a larger percentage of their lives in a captive environment, were better problem-solvers than those that arrived at a later age to the sanctuary. Thus, rehabilitation and time in captivity contributed to improved physical cognitive skills in sanctuary chimpanzees. Our results highlight the importance of studying intraspecific variation and the effect that previous experience and living conditions might have on physical cognitive skills in non-human apes. Accordingly, we should be cautious when extrapolating findings of cognitive studies from one population to the species as a whole.

The technical reasoning hypothesis does not rule out the potential key roles of imitation and working memory for CTC.

To support their claim for technical reasoning skills rather than imitation as the key for cumulative technological culture (CTC), Osiurak and Reynaud argue that chimpanzees can imitate mechanical actions, but do not have CTC. They also state that an increase in working memory in human evolution could not have been a key driver of CTC. We discuss why we disagree with these claims.

Examining the mechanisms underlying the acquisition of animal tool behaviour.

Despite major advances in the study of animal tool behaviour, researchers continue to debate how exactly certain behaviours are acquired. While specific mechanisms, such as genetic predispositions or action copying, are sometimes suspected to play a major role in behavioural acquisition, controlled experiments are required to provide conclusive evidence. In this opinion piece, we refer to classic ethological methodologies to emphasize the need for studying the relative contributions of different factors to the emergence of specific tool behaviours. We describe a methodology, consisting of a carefully staged series of baseline and social-learning conditions, that enables us to tease apart the roles of different mechanisms in the development of behavioural repertoires. Experiments employing our proposed methodology will not only advance our understanding of animal learning and culture, but as a result, will also help inform hypotheses about human cognitive, cultural and technological evolution. More generally, our conceptual framework is suitable for guiding the detailed investigation of other seemingly complex animal behaviours.

Establishing an infrastructure for collaboration in primate cognition research.

Inferring the evolutionary history of cognitive abilities requires large and diverse samples. However, such samples are often beyond the reach of individual researchers or institutions, and studies are often limited to small numbers of species. Consequently, methodological and site-specific-differences across studies can limit comparisons between species. Here we introduce the ManyPrimates project, which addresses these challenges by providing a large-scale collaborative framework for comparative studies in primate cognition. To demonstrate the viability of the project we conducted a case study of short-term memory. In this initial study, we were able to include 176 individuals from 12 primate species housed at 11 sites across Africa, Asia, North America and Europe. All subjects were tested in a delayed-response task using consistent methodology across sites. Individuals could access food rewards by remembering the position of the hidden reward after a 0, 15, or 30-second delay. Overall, individuals performed better with shorter delays, as predicted by previous studies. Phylogenetic analysis revealed a strong phylogenetic signal for short-term memory. Although, with only 12 species, the validity of this analysis is limited, our initial results demonstrate the feasibility of a large, collaborative open-science project. We present the ManyPrimates project as an exciting opportunity to address open questions in primate cognition and behaviour with large, diverse datasets.

Chimpanzee extractive foraging with excavating tools: Experimental modeling of the origins of human technology.

It is hypothesized that tool-assisted excavation of plant underground storage organs (USOs) played an adaptive role in hominin evolution and was also once considered a uniquely human behavior. Recent data indicate that savanna chimpanzees also use tools to excavate edible USOs. However, those chimpanzees remain largely unhabituated and we lack direct observations of this behavior in the wild. To fill this gap in our knowledge of hominoid USO extractive foraging, we conducted tool-mediated excavation experiments with captive chimpanzees naïve to this behavior. We presented the chimpanzees with the opportunity to use tools in order to excavate artificially-placed underground foods in their naturally forested outdoor enclosure. No guidance or demonstration was given to the chimpanzees at any time. The chimpanzees used tools spontaneously in order to excavate the underground foods. They exhibited six different tool use behaviors in the context of excavation: probe, perforate, dig, pound, enlarge and shovel. However, they still excavated manually more often than they did with tools. Chimpanzees were selective in their choice of tools that we provided, preferring longer tools for excavation. They also obtained their own tools mainly from naturally occurring vegetation and transported them to the excavation site. They reused some tools throughout the study. Our new data provide a direction for the study of variables relevant to modeling USO extractive foraging by early hominins.

Animal Behavior: Ape Curiosity on Camera.

How animals respond to novel objects may reflect their overall cognitive and behavioral disposition. A study using camera traps reveals that different species of wild ape respond to novelty differently.

Preferential hand use by captive chimpanzees (Pan troglodytes) in manual and tool digging.

Digging for underground storage organs of plants has been reported in various populations of wild chimpanzees (Pan troglodytes). However, it is unknown so far whether chimpanzees display lateral biases in manual digging as direct observations of this behavior are still lacking. It was therefore the aim of the present study to assess, for the first time, hand preferences for digging in a group of nine captive chimpanzees. We found that with only one exception, all individuals engaged in manual digging for buried food. Five individuals displayed a significant right-hand preference, two a significant left-hand preference, and one was ambidextrous. No apparent differences between males and females were found with regard to the direction or strength of hand preferences for manual digging. Only one out of four parent-offspring pairs was congruent in their preferred hand for manual digging. Three of the eight chimpanzees who dug manually also used tools in order to excavate buried food. Among those three individuals, one displayed a significant right-, one a significant left-hand preference, and one was ambidextrous. Only one of these three chimpanzees was consistent in preferring the same hand for manual and tool digging. The present findings are in line with the notion that chimpanzees display significant hand preferences at the individual level for haptic-guided behaviors, with a tendency for the right hand.

Differences in novel food response between Pongo and Pan.

The diversity of great ape diets requires behavioral flexibility. Consequently, the exploration of potentially novel food sources is supposedly beneficial, but simultaneously, apes show high neophobia to prevent harmful and poisonous food intake. Social information, such as presence of group members or observations of non-naïve, experienced individuals have been demonstrated to affect the acceptance of novel food items in primates. Sociality may have evolutionary effects on the response of apes to novel foods. Here we assess the social information hypothesis, which predicts that selection favors higher neophobia in species where social information is abundant. We report the results from 134 great apes housed in multiple facilities from four closely related species that naturally differ in their degree of sociality: Pongo pygmaeus, Pongo abelii, Pan troglodytes and Pan paniscus. We examined individuals' reactions to novel foods when alone, which enabled us to detect any inherent differences and revealed significant distinctions between species. Chimpanzees and bonobos, that are naturally exposed to higher amounts of social information, were less likely to consume novel foods alone (showed higher neophobia) than the two more solitary orangutan species. Chimpanzees were especially cautious and showed higher explorative behaviors before tasting novel food than other species. Age influenced neophobia as younger individuals of all species took longer to taste novel foods than adults did.

Hand preferences in two unimanual and two bimanual coordinated tasks in the black-handed spider monkey (Ateles geoffroyi).

Spider monkeys are interesting to study with regard to hand preferences, as they are one of the few primate species that lack a thumb and, thus, are unable to perform a precision grip. Further, being platyrrhine primates, they also largely lack independent motor control of the digits and, thus, have only limited manual dexterity. It was therefore the aim of the present study to assess hand preferences in black-handed spider monkeys (Ateles geoffroyi) in 4 tasks differing in task demand: simple unimanual reaching for food and 3 versions of the widely used tube task, including 2 bimanual versions that differ from each other in the degree of fine motor control needed and a unimanual version that does not require coordinated action of the hands. We found that black-handed spider monkeys display significant hand preferences at the individual, but not at the population, level. This was true both in the 2 bimanual coordinated tasks and in the 2 unimanual tasks. Further, our results show that the majority of animals were consistent in the hand they preferred in these 4 tasks. Our findings only partially support the notion that task demand positively correlates with strength of hand preference. Finally, we found that the index finger was the most frequently used digit in all 3 tube tasks, although the animals also used other digits and 2- and 3-finger combinations to extract food from a tube. We conclude that limited manual dexterity does not prevent spider monkeys from displaying strong and consistent hand preferences at the individual level. (PsycINFO Database Record