How does stone-tool use emerge? Introduction of stones and nuts to naïve chimpanzees in captivity

Nut-cracking behavior has been reported in several communities in West Africa but not in East and Central Africa. Furthermore, even within nut-cracking communities, there are individuals who do not acquire the skill. The present study aimed to clarify the cognitive capability required for nut-cracking behavior and the process through which the the nut-cracking behavior emerges. To examine emergence, we provided three naïve adult chimpanzees with a single opportunity to observe human models. A human tester demonstrated nut-cracking behavior using a pair of stones and then supplied stones and nuts to the chimpanzee subjects. Two out of three chimpanzees proceeded to hit a nut on an anvil stone using a hammer stone, one of whom succeeded in cracking open the nuts during the first test session. The third chimpanzee failed to crack open nuts. We used four variables (object, location, body part used, and action) to describe stone/nut manipulation in order to analyze further the patterns of object manipulation exhibited by the subjects. The analysis revealed that there were three main difficulties associated with nut-cracking behavior. (1) The chimpanzee who failed at the task never showed hitting action. (2) The chimpanzee who failed at the task manipulated nuts but rarely stones. (3) The combination of three objects was not commonly observed in the three chimpanzees. We also discuss our results with reference to the effect of enculturation in captivity and the social context of learning in the wild.     

Substrate optimization in nut cracking by capuchin monkeys (Cebus apella)

We conducted an experiment to examine the effect of substrate on the nut-cracking behavior of a group of semicaptive capuchin monkeys. We wanted to determine whether tufted capuchin monkeys were selective in choosing the substrate on which they pound nuts, and whether the choice of substrate affected the outcome. Eight adult females and eight juveniles were provided with nuts in the outdoor facility. We found that 1) all adult females and three young capuchins succeeded in cracking nuts; 2) they preferred the hardest substrates (concrete and stone); 3) there is a link between the substrate and the amount of time needed to crack a nut; 4) most young capuchins used various substrates, some of which were inadequate, in a haphazard manner; and 5) there are different forms of nut cracking. We conclude that adult capuchins choose the hardest substrates, and that these substrates support efficient cracking.     

Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools

We conducted an exploratory investigation in an area where nut-cracking by wild capuchin monkeys is common knowledge among local residents. In addition to observing male and female capuchin monkeys using stones to pound open nuts on stone "anvils," we surveyed the surrounding area and found physical evidence that monkeys cracked nuts on rock outcrops, boulders, and logs (collectively termed anvils). Anvils, which were identified by numerous shallow depressions on the upper surface, the presence of palm shells and debris, and the presence of loose stones of an appropriate size to pound nuts, were present even on the tops of mesas. The stones used to crack nuts can weigh >1 kg, and are remarkably heavy for monkeys that weigh <4 kg. The abundance of shell remains and depressions in the anvil surface at numerous anvil sites indicate that nut-cracking activity is common and long-enduring. Many of the stones found on anvils (presumably used to pound nuts) are river pebbles that are not present in the local area we surveyed (except on or near the anvils); therefore, we surmise that they were transported to the anvil sites. Ecologically and behaviorally, nut-cracking by capuchins appears to have strong parallels to nut-cracking by wild chimpanzees. The presence of abundant anvil sites, limited alternative food resources, abundance of palms, and the habit of the palms in this region to produce fruit at ground level all likely contribute to the monkeys' routine exploitation of palm nuts via cracking them with stones. This discovery provides a new reference point for discussions regarding the evolution of tool use and material culture in primates. Routine tool use to exploit keystone food resources is not restricted to living great apes and ancestral hominids.     

Adult and juvenile bearded capuchin monkeys handle stone hammers differently during nut-cracking

Wild bearded capuchin monkeys (Sapajus libidinosus) habitually use stone hammers to crack open palm nuts and seeds on anvils. This activity requires strength, balance, and precise movement of a large stone with respect to the item placed on an anvil. We explored how well young monkeys cope with these challenges by examining their behavior and the behavior of adults while they cracked palm nuts using a stone. Using video records, we compared actions of six juvenile (2–5 years) and six adult (7+ years) wild monkeys during their first 20 strikes with one unfamiliar ellipsoid, quartzite stone (540 g), and the outcomes of these strikes. Compared with adults, juveniles cracked fewer nuts, performed a more diverse set of exploratory actions, and less frequently placed one or both hands on top of the stone on the downward motion. Adults and juveniles displayed similar low frequencies of striking with a slanted trajectory, missing the nut, and losing control over the nut or stone after striking. These findings indicate that young monkeys control the trajectory of a stone adequately but that is not sufficient to crack nuts as effectively as adults do. Compared with juveniles, adults more quickly perceive how to grip the stone efficiently, and they are able to adjust their grip dynamically during the strike. Young monkeys develop expertise in the latter aspects of cracking nuts over the course of several years of regular practice, indicating that perceptual learning about these aspects of percussion occurs slowly. Juvenile and adult humans learning to use stones to crack nuts also master these features of cracking nuts very slowly.     

Human-induced rapid environmental change: A case study showing negative impact on animal culture

Changes in land use in recent decades have caused substantial biodiversity loss. Some authors suggest that animal cultures could be threatened by human pressure. The tradition of nut-cracking has been thoroughly studied since 2005 in the capuchin monkeys (S. libidinosus) of Fazenda Boa Vista (FBV). Despite being a relatively well-preserved area, the advance of intensive monocultures in the proximity of FBV, among other factors, may have affected the environmental features of the region. In this contribution we investigated the hypothesis that the tradition of nut-cracking using stone tools by bearded capuchin monkeys at FBV is threatened by the rapid transformation of the habitat. We analyzed longitudinal climatic data (mean maximum and minimum temperature and mean maximum and minimum humidity) from 2006 to 2020, and data from the periods 2006–2010 and 2015–2020 for the variables related to nut-cracking: availability of palm trees bearing fruits, ground use and consumption of palm nuts by the monkeys. We show an increase in maximum temperature and a decrease in minimum temperature and minimum humidity over the study years. There was a sharp drop in the number of fruiting palm trees per hectare between the two study periods and a decrease in the time that monkeys spent on the ground, eating palm nuts, and nut-cracking with tools. We confirmed the hypothesis that the tradition of using tools in feeding is threatened. Our results show that in less than two decades, habitat anthropization already negatively impacts animal cultures. We emphasize the importance of considering behavioral diversity in conservation criteria.     

Nut-like oil seeds: food for monkeys, chimpanzees, humans, and probably ape-men

The hypothetical hyperrobust australopithecine gnathic nutcracker adaptation is reexamined in light of ecobotanical information on edible wild nuts provided by the flora of tropical and subtropical Africa. The nut producing species are tree-forms. Those of the forest region do not as a rule produce fruits with edible mesocarps. In contrast, the woodland savanna species (particularly in the Zambezian region) characteristically provide an important whole fruit, i.e., a nutritious mesocarp in addition to edible oil-rich nut seeds. These fruits drop from the tree before they are fully mature and go through the final ripening phase on the ground. They are important seasonal foods for a variety of vertebrates, including primates, elephants, and antelope. Altogether the nuts exhibit a broad range of toughness values, measured here as strength under compression. The woodland nuts are not as tough (177-934 kg force, breaking load) as those of the tropical forest (192-1,673 kg force). The seed-predators of the woodland species include squirrels, baboons, warthogs, and parrots. Paleoecological analyses indicate that it was the woodland nuts that were probably available to Australopithecus boisei and A. robustus. Preliminary estimates of adult male gnathic nut-cracking capabilities suggest that A. boisei could have orally cracked a significant portion of the woodland nuts. In spite of this, ecobotanical data indicate that we can probably reject the hypothesis that these hominids were year-round gnathic nut-cracking specialists. Both the indirect and direct evidence support this conclusion.     

Preliminary assessment of methods used to demonstrate nut-cracking behavior to five captive chimpanzees (Pan troglodytes)

Chimpanzees acquire nut-cracking skills by observation and trial and error. Studies of captive chimpanzees have shown the effectiveness of a skilled demonstrator. We examined the effectiveness of 3 live demonstration forms from which subjects could learn nut-cracking skills: a video of proficient conspecifics, human demonstration and the presence of a skilled conspecific performing the task. A male subject did not learn to crack open nuts after viewing a video of proficient conspecifics but quickly learned the skill following a demonstration by a human facilitator. Subsequently, 4 female chimpanzees were given the opportunity to learn the skill from the now proficient male, as well as from a video and human demonstration, but failed to do so.     

Chimpanzees using stones to crack open oil palm nuts in Liberia

The use of stone-tools to open palm nuts (Elaeis guineensis) was studied in a group of 16 chimpanzees (Pan troglodytes) released from captivity to a natural island setting in Liberia. The behaviour was started by one female of the group; it then spread to 12 others over periods varying from a few seconds to a few weeks. Nut-cracking soon spread to three other sites, both spontaneously and with human encouragement. Both nuts and tools were carried distances of several hundred meters. Social interaction at cracking sites was rich and varied, ranging from fights over possession of tools to unsolicited sharing of nuts. Nut-crackers showed selectivity in schoosing “good” nuts and varied their methods according to the qualities of the nuts. Individual differences in technique emerged. These are the first detailed behavioural data on palm-nut-cracking, and they show many parallels with nut-cracking of other species by chimpanzees of the Tai Forest, Ivory Coast. This is another example of hammer-stone use from a limited region of West Africa: southeastern Guinea, eastern Liberia, and western Ivory Coast. This suggests limited cultural diffusion of the custom.     

Why Don't Chimpanzees in Gabon Crack Nuts?

Some populations of wild chimpanzees (Pan troglodytes) use hammers and anvils of stone or wood to crack open nuts for food. Others do not. The aim of this study was to ask why one non-nut-cracking population, in the Lopé Reserve, Gabon, lacks this useful form of tool use. We tested 10 hypotheses: (1) nuts are absent; (2) nuts are few; (3) nuts are unsuitable; (4) hammers are absent; (5) hammers are unsuitable; (6) anvils are absent; (7) anvils are unsuitable; (8) nuts are displaced by better food items; (9) intelligence is insufficient; and (10) knowledge is insufficient. All but the last are clearly falsified, leaving by exclusion the likelihood that Lopé's chimpanzees lack the technology—knowledge of appropriate technique—to exploit this resource. Thus, the behavioral differences across populations of these apes are cultural and not environmentally dictated. This explanation is congruent with the distribution of chimpanzee nut-cracking across Africa.     

Percussive tool use by Ta? Western chimpanzees and Fazenda Boa Vista bearded capuchin monkeys: a comparison

Percussive tool use holds special interest for scientists concerned with human origins. We summarize the findings from two field sites, Taï and Fazenda Boa Vista, where percussive tool use by chimpanzees and bearded capuchins, respectively, has been extensively investigated. We describe the ecological settings in which nut-cracking occurs and focus on four aspects of nut-cracking that have important cognitive implications, namely selection of tools, tool transport, tool modification and modulation of actions to reach the goal of cracking the nut. We comment on similarities and differences in behaviour and consider whether the observed differences reflect ecological, morphological, social and/or cognitive factors. Both species are sensitive to physical properties of tools, adjust their selection of hammers conditionally to the resistance of the nuts and to transport distance, and modulate the energy of their strikes under some conditions. However, chimpanzees transport hammers more frequently and for longer distances, take into account a higher number of combinations of variables and occasionally intentionally modify tools. A parsimonious interpretation of our findings is that morphological, ecological and social factors account for the observed differences. Confirmation of plausible cognitive differences in nut-cracking requires data not yet available.     

Oil Palm Use by Adjacent Communities of Chimpanzees at Bossou and Nimba Mountains,West Africa

We investigated oil palm (Elaeis guineensis) use for feeding in 3 chimpanzee communities: Bossou and Seringbara in Guinea and Yealé in Côte d'Ivoire. Bossou was used as the benchmark for comparison. Bossou chimpanzees (Pan troglodytes verus) exhibit a wide range of oil palm targeted behaviors. We used direct observations of their two tool use, i.e., nut-cracking and pestle pounding, to establish strict and reliable criteria to ascertain the presence of comparable behaviors at the two adjacent Nimba sites. Based on monthly surveys of oil palms across the three sites, significant differences in patterns of use emerged. Bossou chimpanzees demonstrated the greatest frequency of oil palm use, while Seringbara chimpanzees, 6 km away, failed to exhibit any use and Yealé chimpanzees, 12 km away, showed all uses comparable to Bossou chimpanzees except pestle pounding and mature leaf pith-feeding. We examined the density and distribution of oil palms, tool availability for nut-cracking and pestle pounding, fruit, flower and nut availability, competition with sympatric species for fruit and nuts and the diversity of fruit species in the diet across the 3 sites. We found no clear difference in proximate environmental variables underlying observed variations in oil palm use among the 3 sites, yielding the conclusion that the differences are cultural. Assuming individual interchange between communities and the involvement of social learning in the intracommunity transmission and maintenance of oil palm uses, the result raises interesting questions about diffusion of behavior between neighboring chimpanzee communities.     

Kinematics and energetics of nut-cracking in wild capuchin monkeys (Cebus libidinosus) in Piauí, Brazil

Wild bearded capuchins (Cebus libidinosus, quadrupedal, medium-sized monkeys) crack nuts using large stones. We examined the kinematics and energetics of the nut-cracking action of two adult males and two adult females. From a bipedal stance, the monkeys raised a heavy hammer stone (1.46 and 1.32 kg, from 33 to 77% of their body weight) to an average height of 0.33 m, 60% of body length. Then, they rapidly lowered the stone by flexing the lower extremities and the trunk until the stone contacted the nut. A hit consisting of an upward phase and a downward phase averaged 0.74 s in duration. The upward phase lasted 69% of hit duration. All subjects added discernable energy to the stone in the downward phase. The monkeys exhibited individualized kinematic strategies, similar to those of human weight lifters. Capuchins illustrate that human-like bipedal stance and large body size are unnecessary to break tough objects from a bipedal position. The phenomenon of bipedal nut-cracking by capuchins provides a new comparative reference point for discussions of percussive tool use and bipedality in primates.     

Nocturnal relocation of adult and juvenile coral reef fishes in response to reef noise

Juvenile and adult reef fishes often undergo migration, ontogenic habitat shifts, and nocturnal foraging movements. The orientation cues used for these behaviours are largely unknown. In this study, the use of sound as an orientation cue guiding the nocturnal movements of adult and juvenile reef fishes at Lizard Island, Great Barrier Reef was examined. The first experiment compared the movements of fishes to small patch reefs where reef noise was broadcast, with those to silent reefs. No significant responses were found in the 79 adults that were collected, but the 166 juveniles collected showed an increased diversity each morning on the reefs with broadcast noise, and significantly greater numbers of juveniles from three taxa (Apogonidae, Gobiidae and Pinguipedidae) were collected from reefs with broadcast noise. The second experiment compared the movement of adult and juvenile fishes to reefs broadcasting high (>570 Hz), or low (<570 Hz) frequency reef noise, or to silent reefs. Of the 122 adults collected, the highest diversity was seen at the low frequency reefs; and adults from two families (Gobiidae and Blenniidae) preferred these reefs. A similar trend was observed in the 372 juveniles collected, with higher diversity at the reefs with low frequency noises. This preference was seen in the juvenile apogonids; however, juvenile gobiids were attracted to both high and low sound treatments equally, and juvenile stage Acanthuridae preferred the high frequency noises. This evidence that juvenile and adult reef fishes orientate with respect to the soundscape raises important issues for management, conservation and the protection of sound cues used in natural behaviour.     

The Influence of Social Environment: Behavior of Unrelated Adults Affects Future Juvenile Behaviors

Juveniles' behaviors are often influenced by the behaviors of conspecifics. Most experimental studies of the influence of conspecific behavior vary the social environment by the presence or absence of conspecifics or investigate the impact of the outcome of social encounters (winner/loser effects) but less frequently expose individuals to variation in behavioral phenotypes present in the social environment. Based on previous work showing that juveniles of the salamander Plethodon cinereus are likely to interact frequently with non‐parental adults, I hypothesized that territorial adults in the social environment alter the future behaviors of juveniles. I measured the intracohort social behaviors of juvenile salamanders collected from two geographic areas, Michigan (MI) and Virginia (VA), before and after housing with ostensibly territorial (VA) or non‐territorial (MI) adults. There were overall effects of adult territoriality and aggression on the behavior of juveniles. However, juveniles from populations in MI were especially susceptible to behavioral modification. Compared with behaviors prior to being housed with adults, MI juveniles increased investigatory and escape behaviors in juvenile–juvenile interactions after being housed with adults that displayed territorial behaviors and decreased investigatory and escape behaviors after being housed with non‐territorial adults. This study shows that not only is a specific behavior, territoriality of adult salamanders, a social environment that modifies future juvenile behaviors, but the effects of social environment may differ between populations.     

Social behaviour of juvenile red sea urchins, Strongylocentrotus franciscanus (Agassiz)

This study examined social behaviour of juvenile red sea urchins, Strongylocentrotus franciscanus (Agassiz). At four coastal locations in British Columbia, Canada, distributions of juvenile sea urchins were examined in relation to adults. One-third of all juveniles were found underneath an adult “spine canopy”, another third outside the spine canopy but close to an adult, and the remainder were found apart from adults. Juveniles associated with adults were contagiously distributed with each other. In the laboratory, juveniles chose adults over other target locations. They selected adults in particular locations over others, and in one case showed selection among adults; but they did not select between fed and non-fed adults, nor between adults that had been “protective” and “non-protective” of juveniles in the field. In time-lapse film studies, starved juveniles showed little change in social behaviour when food was introduced, but showed a dramatic change in behaviour when predators were active. We suggest that juvenile red sea urchins are found under the spine canopies of adults as a result of juvenile behaviour; and that this interaction functions to protect juveniles from predation. The strong gregarious nature of juveniles among themselves may have evolved in a different selective situation as a defence against predation and to ensure reproductive success.     

Handedness in wild chimpanzees

The debate over nonhuman primate precursors to human handedness is unsettled mainly due to lack of data, particularly on apes. Handedness in wild chimpanzees at the Taï National Park Côte d'Ivoire, has been monitored in four tasks. For the simple unimanual ones, reaching and grooming, adults use both hands equally (ambidextrous), while for the more complex unimanual wadge-dipping and the complex bimanual nut-cracking, adults are highly lateralized. These results support the hypothesis that lateralization increases with the complexity of the task. The lateralization is constant for years for each task but may vary in an individual with respect to different tasks. For nutcracking females are more lateralized than males. The ontogeny of handedness for nut-cracking shows many variations in the tendency to use one hand and in the side preferred, until at about 10 years of age, the individual achieves her adult handedness. No population bias toward one side exists in Taï chimpanzees. No heritability of handedness between mother and offspring was observed. Human and chimpanzees handedness are compared.     

Interactions between year classes in the benthic amphipod Monoporeia affinis: effects on juvenile survival and growth

Summary The effect of 1-year-old Monoporeia (=Pontoporeia) affinis on the survival and growth of young of the year was studied in laboratory experiments. Amphipods were kept in jars with sediment and a continuous supply of cooled water for 3 months. Adults or juveniles were added to a control density of juveniles. Juvenile mortality increased at higher total densities, and was greater when adults were present. The mean length and dry weight of juveniles decreased at higher densities, but adults did not have a greater effect than juveniles. These density-dependent effects are probably caused by competition for food within and between year classes. Thus, a high abundance of juveniles or adults could reduce the recruitment of juveniles into the adult year-class the following year, and the suppression of juvenile growth could lower fecundity. The results of this experiment support the hypothesis, inferred from field data from the Baltic Sea and Swedish lakes, that intraspecific interactions contribute to fluctuations in the abundance of populations of M. affinis.     

Ontogeny of auditory saccular sensitivity in the plainfin midshipman fish, <Emphasis Type="Italic">Porichthys notatus</Emphasis>

The auditory system of the plainfin midshipman fish, Porichthys notatus, is an important sensory receiver system used to encode intraspecific social communication signals in adults, but the response properties and function of this receiver system in pre-adult stages are less known. In this study we examined the response properties of auditory-evoked potentials from the midshipman saccule, the main organ of hearing in this species, to determine whether the frequency response and auditory threshold of saccular hair cells to behaviorally relevant single tone stimuli change during ontogeny. Saccular potentials were recorded from three relative sizes of midshipman fish: small juveniles [1.9–3.1 cm standard length (SL), large juveniles (6.8–8.0 cm SL) and non-reproductive adults (9.0–22.6 cm SL)]. The auditory evoked potentials were recorded from the rostral, middle and caudal regions of the saccule while single tone stimuli (75–1,025 Hz) were presented via an underwater speaker. We show that the frequency response and auditory threshold of the midshipman saccule is established early in development and retained throughout ontogeny. We also show that saccular sensitivity to frequencies greater than 385 Hz increases with age/size and that the midshipman saccule of small and large juveniles, like that of non-reproductive adults, is best suited to detect low frequency sounds (<105 Hz) in their natural acoustic environment.     

Extended Mother–Offspring Relationships in Crayfish: The Return Behaviour of Juvenile Procambarus Clarkii

Crayfish shows a relatively complex parental behaviour compared with other invertebrates, but the literature provides only anecdotal accounts of this phenomenon. In Procambarus clarkii, we described the ‘return’ behaviour of third‐stage juveniles when offered four types of adults: biological mothers, foster mothers, non‐brooding females and males. Then, we analysed the posture and behaviour of the adults to understand the role played by the putative mother in attracting the juveniles. Contrary to non‐brooding individuals, both biological and foster mothers displayed a relatively rare locomotion, executed few cleaning and feeding acts, and never attempted to prey on juveniles. They often assumed a ‘spoon‐like telson posture’ that seemed to facilitate offspring’s approaches. Juveniles increased the frequency of tail‐flips away in the presence of non‐brooding adults; conversely, they accepted foster mothers, along with biological mothers, but not as fast as the latter. Taken together, these results suggest that mother–offspring relationships in P. clarkii are more refined than previously thought, being possibly a key factor enabling this species to thrive in harsh environmental conditions.     

Dietary responses to fruit scarcity of wild chimpanzees at Bossou,Guinea: Possible implications for ecological importance of tool use

A 13-month ecological study was conducted at Bossou, Guinea, West Africa, to elucidate how a community of wild chimpanzees (Pan troglodytes verus) deals with the scarcity of main foods. During the study period, fruit availability fluctuated radically. The chimpanzees were confirmed to depend heavily on three “keystone resources” which were available when their main foods (fruit pulp) were scarce. These were fruits of Musanga cecropioides, oil-palm (Elaeis guineensis) nuts, and oil-palm pith. These are abundant in the chimpanzees' home range and their nutritional contents compensate for a decrease in nutritional intake from fruit pulp. The presence of these excellent backup foods may explain the high reproductive performance of Bossou chimpanzees. Here, chimpanzees consumed two of the three keystone foods using two types of tool behavior: nut-cracking for oil-palm nuts and pestle-pounding for oil-palm pith. These tool-using behaviors accounted for 31.9% of the total feeding time spent in June (the month in which the highest frequency occurred) and 10.4% in total for the year. It is suggested that the Bossou chimpanzees depend strongly on tools for their subsistence. This implies a possible function for tool technology in the evolution of our human ancestors. Am J Phys Anthropol 106:283–295, 1998. © 1998 Wiley-Liss, Inc.