Genetic and ‘cultural’ similarity in wild chimpanzees

The question of whether animals possess ‘cultures’ or ‘traditions’ continues to generate widespread theoretical and empirical interest. Studies of wild chimpanzees have featured prominently in this discussion, as the dominant approach used to identify culture in wild animals was first applied to them. This procedure, the ‘method of exclusion,’ begins by documenting behavioural differences between groups and then infers the existence of culture by eliminating ecological explanations for their occurrence. The validity of this approach has been questioned because genetic differences between groups have not explicitly been ruled out as a factor contributing to between-group differences in behaviour. Here we investigate this issue directly by analysing genetic and behavioural data from nine groups of wild chimpanzees. We find that the overall levels of genetic and behavioural dissimilarity between groups are highly and statistically significantly correlated. Additional analyses show that only a very small number of behaviours vary between genetically similar groups, and that there is no obvious pattern as to which classes of behaviours (e.g. tool-use versus communicative) have a distribution that matches patterns of between-group genetic dissimilarity. These results indicate that genetic dissimilarity cannot be eliminated as playing a major role in generating group differences in chimpanzee behaviour.     

Design complexity in termite-fishing tools of chimpanzees (Pan troglodytes)

Adopting the approach taken with New Caledonian crows (Corvus moneduloides), we present evidence of design complexity in one of the termite-fishing tools of chimpanzees (Pan troglodytes) in the Goualougo Triangle, Republic of Congo. Prior to termite fishing, chimpanzees applied a set of deliberate, distinguishable actions to modify herb stems to fashion a brush-tipped probe, which is different from the form of fishing tools used by chimpanzees in East and West Africa. This means that ‘brush-tipped fishing probes’, unlike ‘brush sticks’, are not a by-product of use but a deliberate design feature absent in other chimpanzee populations. The specialized modifications to prepare the tool for termite fishing, measures taken to repair non-functional brushes and appropriate orientation of the modified end suggest that these wild chimpanzees are attentive to tool modifications. We also conducted experimental trials that showed that a brush-tipped probe is more effective in gathering insects than an unmodified fishing probe. Based on these findings, we suggest that chimpanzees in the Congo Basin have developed an improved fishing probe design.     

How similar are nut-cracking and stone-flaking? A functional approach to percussive technology

Various authors have suggested similarities between tool use in early hominins and chimpanzees. This has been particularly evident in studies of nut-cracking which is considered to be the most complex skill exhibited by wild apes, and has also been interpreted as a precursor of more complex stone-flaking abilities. It has been argued that there is no major qualitative difference between what the chimpanzee does when he cracks a nut and what early hominins did when they detached a flake from a core. In this paper, similarities and differences between skills involved in stone-flaking and nut-cracking are explored through an experimental protocol with human subjects performing both tasks. We suggest that a ‘functional’ approach to percussive action, based on the distinction between functional parameters that characterize each task and parameters that characterize the agent''s actions and movements, is a fruitful method for understanding those constraints which need to be mastered to perform each task successfully, and subsequently, the nature of skill involved in both tasks.     

Theft in an ultimatum game: chimpanzees and bonobos are insensitive to unfairness

Humans, but not chimpanzees, punish unfair offers in ultimatum games, suggesting that fairness concerns evolved sometime after the split between the lineages that gave rise to Homo and Pan. However, nothing is known about fairness concerns in the other Pan species, bonobos. Furthermore, apes do not typically offer food to others, but they do react against theft. We presented a novel game, the ultimatum theft game, to both of our closest living relatives. Bonobos and chimpanzee ‘proposers’ consistently stole food from the responders'' portions, but the responders did not reject any non-zero offer. These results support the interpretation that the human sense of fairness is a derived trait.     

Baboons, chimpanzees, and tools

Wild chimpanzees make and use tools with far greater frequency and variety than wild baboons. Sampling differences; differences in the sensory, motor, or cognitive capacities for skilled tool use; or environmental differences are not responsible. Fortuitous discovery of novel forms of tool behavior probably occurs as rarely among chimpanzees as among baboons. However, research on wild and captive chimpanzees reveals that the discovery is transmitted quickly among chimpanzee groups by observation learning, and thus becomes well-established in the group's behavioral repertoire. In contrast, study of captive baboons reveals that they acquire little information about tool behavior by observation. With little observation learning the behavior is not likely to be acquired by other group members since repeated independent discovery is improbable. Thus chimpanzees' more proficient tool behavior is due mainly to their greater capacity for observation learning. This suggests that the advent of hominid tool traditions was accompanied by a capacity for facile observation learning and thus, perhaps, by language ability.     

When maths trumps logic: probabilistic judgements in chimpanzees

When searching for hidden food, do chimpanzees take into account both the number of hidden items and the number of potential hiding locations? We presented chimpanzees with two trays, each of them containing a different food/cup ratio and therefore a different likelihood of finding a baited cup among empty alternatives. Subjects'' performance was directly influenced by the relative difference (probability ratio (PR)) between the two given probabilities. Interestingly, however, they did not appreciate the special value of a truly safe option (with P = 1.0). Instead, they seemed to ‘blindly’ rely on the PR between the two options, systematically preferring the more likely one once a certain threshold had been reached. A control condition ruled out the possibility of low-level learning explanations for the observed performance.     

‘Adoption’ by Maternal Siblings in Wild Chimpanzees

The adoption of unrelated orphaned infants is something chimpanzees and humans have in common. Providing parental care has fitness implications for both the adopter and orphan, and cases of adoption have thus been cited as evidence for a shared origin of an altruistic behaviour. We provide new data on adoptions in the free-living Sonso chimpanzee community in Uganda, together with an analysis of published data from other long-term field sites. As a default pattern, we find that orphan chimpanzees do not become adopted by adult group members but wherever possible associate with each other, usually as maternal sibling pairs. This occurs even if both partners are still immature, with older individuals effectively becoming ‘child household heads’. Adoption of orphans by unrelated individuals does occur but usually only if no maternal siblings or other relatives are present and only after significant delays. In conclusion, following the loss of their mother, orphaned chimpanzees preferentially associate along pre-existing social bonds, which are typically strongest amongst maternal siblings.     

Genetic composition of social groups influences male aggressive behaviour and fitness in natural genotypes of Drosophila melanogaster

Indirect genetic effects (IGEs) describe how an individual''s behaviour—which is influenced by his or her genotype—can affect the behaviours of interacting individuals. IGE research has focused on dyads. However, insights from social networks research, and other studies of group behaviour, suggest that dyadic interactions are affected by the behaviour of other individuals in the group. To extend IGE inferences to groups of three or more, IGEs must be considered from a group perspective. Here, I introduce the ‘focal interaction’ approach to study IGEs in groups. I illustrate the utility of this approach by studying aggression among natural genotypes of Drosophila melanogaster. I chose two natural genotypes as ‘focal interactants’: the behavioural interaction between them was the ‘focal interaction’. One male from each focal interactant genotype was present in every group, and I varied the genotype of the third male—the ‘treatment male’. Genetic variation in the treatment male''s aggressive behaviour influenced the focal interaction, demonstrating that IGEs in groups are not a straightforward extension of IGEs measured in dyads. Further, the focal interaction influenced male mating success, illustrating the role of IGEs in behavioural evolution. These results represent the first manipulative evidence for IGEs at the group level.     

Predicting the Vulnerability of Great Apes to Disease: The Role of Superspreaders and Their Potential Vaccination

Disease is a major concern for the conservation of great apes, and one that is likely to become increasingly relevant as deforestation and the rise of ecotourism bring humans and apes into ever closer proximity. Consequently, it is imperative that preventative measures are explored to ensure that future epidemics do not wipe out the remaining populations of these animals. In this paper, social network analysis was used to investigate vulnerability to disease in a population of wild orang-utans and a community of wild chimpanzees. Potential ‘superspreaders’ of disease - individuals with disproportionately central positions in the community or population - were identified, and the efficacy of vaccinating these individuals assessed using simulations. Three resident female orang-utans were identified as potential superspreaders, and females and unflanged males were predicted to be more influential in disease spread than flanged males. By contrast, no superspreaders were identified in the chimpanzee network, although males were significantly more central than females. In both species, simulating the vaccination of the most central individuals in the network caused a greater reduction in potential disease pathways than removing random individuals, but this effect was considerably more pronounced for orang-utans. This suggests that targeted vaccinations would have a greater impact on reducing disease spread among orang-utans than chimpanzees. Overall, these results have important implications for orang-utan and chimpanzee conservation and highlight the role that certain individuals may play in the spread of disease and its prevention by vaccination.     

Individual acquisition of “stick pounding” behavior by naïve chimpanzees

Many studies investigating culture in nonhuman animals tend to focus on the inferred need of social learning mechanisms that transmit the form of a behavior to explain the population differences observed in wild animal behavioral repertoires. This research focus often results in studies overlooking the possibility of individuals being able to develop behavioral forms without requiring social learning. The disregard of individual learning abilities is most clearly observed in the nonhuman great ape literature, where there is a persistent claim that chimpanzee behaviors, in particular, require various forms of social learning mechanisms. These special social learning abilities have been argued to explain the acquisition of the relatively large behavioral repertoires observed across chimpanzee populations. However, current evidence suggests that although low‐fidelity social learning plays a role in harmonizing and stabilizing the frequency of behaviors within chimpanzee populations, some (if not all) of the forms that chimpanzee behaviors take may develop independently of social learning. If so, they would be latent solutions—behavioral forms that can (re‐)emerge even in the absence of observational opportunities, via individual (re)innovations. Through a combination of individual and low‐fidelity social learning, the population‐wide patterns of behaviors observed in great ape species are then established and stably maintained. This is the Zone of Latent Solutions (ZLS) hypothesis. The current study experimentally tested the ZLS hypothesis for pestle pounding, a wild chimpanzee behavior. We tested the reinnovation of this behavior in semi‐wild chimpanzees at Chimfunshi Wildlife Orphanage in Zambia, Africa, (N = 90, tested in four social groups). Crucially, all subjects were naïve to stick pounding before testing. Three out of the four tested groups reinnovated stick pounding—clearly demonstrating that this behavioral form does not require social learning. These findings provide support for the ZLS hypothesis alongside further evidence for the individual learning abilities of chimpanzees.     

Differences in Learning Volitional (Manual) and Non-Volitional (Posture) Aspects of a Complex Motor Skill in Young Adult Dyslexic and Skilled Readers

The ‘Cerebellar Deficit Theory’ of developmental dyslexia proposes that a subtle developmental cerebellar dysfunction leads to deficits in attaining ‘automatic’ procedures and therefore manifests as subtle motor impairments (e.g., balance control, motor skill learning) in addition to the reading and phonological difficulties. A more recent version of the theory suggests a core deficit in motor skill acquisition. This study was undertaken to compare the time-course and the nature of practice-related changes in volitional (manual) and non-volitional (posture) motor performance in dyslexic and typical readers while learning a new movement sequence. Seventeen dyslexic and 26 skilled young adult readers underwent a three-session training program in which they practiced a novel sequence of manual movements while standing in a quiet stance position. Both groups exhibited robust and well-retained gains in speed, with no loss of accuracy, on the volitional, manual, aspects of the task, with a time-course characteristic of procedural learning. However, the dyslexic readers exhibited a pervasive slowness in the initiation of volitional performance. In addition, while typical readers showed clear and well-retained task-related adaptation of the balance and posture control system, the dyslexic readers had significantly larger sway and variance of sway throughout the three sessions and were less efficient in adapting the posture control system to support the acquisition of the novel movement sequence. These results support the notion of a non-language-related deficit in developmental dyslexia, one related to the recruitment of motor systems for effective task performance rather than to a general motor learning disability.     

Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis

Although monitoring social information is a key aspect of the social complexity hypothesis, surprisingly little work has compared social knowledge across different species of wild animals. In the present study, I use playback experiments to test for individual recognition in wild male geladas (Theropithecus gelada) to compare with published accounts of social knowledge in chacma baboons (Papio ursinus). Geladas and baboons are closely related primates living in socially complex groups that differ dramatically in group size—geladas routinely associate with more than 10 times the number of conspecifics than do baboons. Using grunts from non-rival males to simulate approaches, I examined the strength of a subject male''s response when the ‘approach’ was from the direction of (i) non-rival males (control), or (ii) rival males (a more salient stimulus if playback grunts are not recognized by the subject). I compared responses separately based on the degree of social overlap between the caller and the subject. Responses indicate that male geladas, unlike baboons, do not use vocalizations to recognize all of the individuals they regularly encounter. This represents, to my knowledge, the first documented evidence of ‘missing’ social knowledge in a natural primate population. The sharp distinction between baboons and geladas suggests that geladas are either unable or unmotivated to keep track of the individual identity of other males in their multi-level society—even males with whom they have a large degree of social overlap. Thus, these results are consistent with the central assumption of the social complexity hypothesis that social cognition is costly.     

Neural signatures of betrayal aversion: an fMRI study of trust

Decisions are said to be ‘risky’ when they are made in environments with uncertainty caused by nature. By contrast, a decision is said to be ‘trusting’ when its outcome depends on the uncertain decisions of another person. A rapidly expanding literature reveals economically important differences between risky and trusting decisions, and further suggests these differences are due to ‘betrayal aversion’. While its neural foundations have not been previously illuminated, the prevailing hypothesis is that betrayal aversion stems from a desire to avoid negative emotions that arise from learning one''s trust was betrayed. Here, we provide evidence from an fMRI study that supports this hypothesis. In particular, our data indicate that the anterior insula modulates trusting decisions that involve the possibility of betrayal.     

Simian Immunodeficiency Virus Infection of Chimpanzees (Pan troglodytes) Shares Features of Both Pathogenic and Non-pathogenic Lentiviral Infections

The virus-host relationship in simian immunodeficiency virus (SIV) infected chimpanzees is thought to be different from that found in other SIV infected African primates. However, studies of captive SIVcpz infected chimpanzees are limited. Previously, the natural SIVcpz infection of one chimpanzee, and the experimental infection of six chimpanzees was reported, with limited follow-up. Here, we present a long-term study of these seven animals, with a retrospective re-examination of the early stages of infection. The only clinical signs consistent with AIDS or AIDS associated disease was thrombocytopenia in two cases, associated with the development of anti-platelet antibodies. However, compared to uninfected and HIV-1 infected animals, SIVcpz infected animals had significantly lower levels of peripheral blood CD4+ T-cells. Despite this, levels of T-cell activation in chronic infection were not significantly elevated. In addition, while plasma levels of β2 microglobulin, neopterin and soluble TNF-related apoptosis inducing ligand (sTRAIL) were elevated in acute infection, these markers returned to near-normal levels in chronic infection, reminiscent of immune activation patterns in ‘natural host’ species. Furthermore, plasma soluble CD14 was not elevated in chronic infection. However, examination of the secondary lymphoid environment revealed persistent changes to the lymphoid structure, including follicular hyperplasia in SIVcpz infected animals. In addition, both SIV and HIV-1 infected chimpanzees showed increased levels of deposition of collagen and increased levels of Mx1 expression in the T-cell zones of the lymph node. The outcome of SIVcpz infection of captive chimpanzees therefore shares features of both non-pathogenic and pathogenic lentivirus infections.     

Development of a New Method to Track Multiple Honey Bees with Complex Behaviors on a Flat Laboratory Arena

A computer program that tracks animal behavior, thereby revealing various features and mechanisms of social animals, is a powerful tool in ethological research. Because honeybee colonies are populated by thousands of bees, individuals co-exist in high physical densities and are difficult to track unless specifically tagged, which can affect behavior. In addition, honeybees react to light and recordings must be made under special red-light conditions, which the eyes of bees perceive as darkness. The resulting video images are scarcely distinguishable. We have developed a new algorithm, K-Track, for tracking numerous bees in a flat laboratory arena. Our program implements three main processes: (A) The object (bee''s) region is detected by simple threshold processing on gray scale images, (B) Individuals are identified by size, shape and spatiotemporal positional changes, and (C) Centers of mass of identified individuals are connected through all movie frames to yield individual behavioral trajectories. The tracking performance of our software was evaluated on movies of mobile multi-artificial agents and of 16 bees walking around a circular arena. K-Track accurately traced the trajectories of both artificial agents and bees. In the latter case, K-track outperformed Ctrax, well-known software for tracking multiple animals. To investigate interaction events in detail, we manually identified five interaction categories; ‘crossing’, ‘touching’, ‘passing’, ‘overlapping’ and ‘waiting’, and examined the extent to which the models accurately identified these categories from bee''s interactions. All 7 identified failures occurred near a wall at the outer edge of the arena. Finally, K-Track and Ctrax successfully tracked 77 and 60 of 84 recorded interactive events, respectively. K-Track identified multiple bees on a flat surface and tracked their speed changes and encounters with other bees, with good performance.     

Bonobos and chimpanzees exhibit human-like framing effects

Humans exhibit framing effects when making choices, appraising decisions involving losses differently from those involving gains. To directly test for the evolutionary origin of this bias, we examined decision-making in humans'' closest living relatives: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We presented the largest sample of non-humans to date (n = 40) with a simple task requiring minimal experience. Apes made choices between a ‘framed’ option that provided preferred food, and an alternative option that provided a constant amount of intermediately preferred food. In the gain condition, apes experienced a positive ‘gain’ event in which the framed option was initially presented as one piece of food but sometimes was augmented to two. In the loss condition, apes experienced a negative ‘loss'' event in which they initially saw two pieces but sometimes received only one. Both conditions provided equal pay-offs, but apes chose the framed option more often in the positive ‘gain’ frame. Moreover, male apes were more susceptible to framing than were females. These results suggest that some human economic biases are shared through common descent with other apes and highlight the importance of comparative work in understanding the origins of individual differences in human choice.     

Automatic imitation in dogs

After preliminary training to open a sliding door using their head and their paw, dogs were given a discrimination task in which they were rewarded with food for opening the door using the same method (head or paw) as demonstrated by their owner (compatible group), or for opening the door using the alternative method (incompatible group). The incompatible group, which had to counterimitate to receive food reward, required more trials to reach a fixed criterion of discrimination performance (85% correct) than the compatible group. This suggests that, like humans, dogs are subject to ‘automatic imitation’; they cannot inhibit online the tendency to imitate head use and/or paw use. In a subsequent transfer test, where all dogs were required to imitate their owners'' head and paw use for food reward, the incompatible group made a greater proportion of incorrect, counterimitative responses than the compatible group. These results are consistent with the associative sequence learning model, which suggests that the development of imitation depends on sensorimotor experience and phylogenetically general mechanisms of associative learning. More specifically, they suggest that the imitative behaviour of dogs is shaped more by their developmental interactions with humans than by their evolutionary history of domestication.     

Genetic Diversity of and Differentiation among Five Populations of Blunt Snout Bream (Megalobrama amblycephala) Revealed by SRAP Markers: Implications for Conservation and Management

The blunt snout bream (Megalobrama amblycephala) is an important freshwater aquaculture fish throughout China. Because of widespread introductions of this species to many regions, the genetic diversity of wild and natural populations is now threatened. In the present study, SRAP (sequence-related amplified polymorphism) markers were used to assess genetic diversity of blunt snout bream. Three natural populations (Liangzi Lake, Poyang Lake and Yuni Lake, one cultured population (Nanxian) and one genetic strain (‘Pujiang No. 1’) of blunt snout bream were screened with 88 SRAP primer combinations, of which 13 primer pairs produced stable and reproducible amplification patterns. In total, 172 bands were produced, of which 132 bands were polymorphic. Nei''s gene diversity (h) and Shannon''s information index (I) values provided evidence of differences in genetic diversity among the five populations (Poyang Lake>Liangzi Lake>Nanxian>‘Pujiang No. 1’>Yuni Lake). Based on cluster analysis conducted on genetic distance values, the five blunt snout bream populations were divided into three groups, Poyang Lake and Liangzi Lake (natural populations), Nanxian and ‘Pujiang No. 1’ (cultured population and genetically selected strain), and Yuni Lake (natural population). Significant genetic differentiation was found among the five populations using analysis of molecular variance (AMOVA), with more genetic divergence existing among populations (55.49%), than within populations (44.51%). This molecular marker technique is a simple and efficient method to quantify genetic diversity within and among fish populations, and is employed here to help manage and conserve germplasm variability of blunt snout bream and to support the ongoing selective breeding programme for this fish.     

Tool use by wild chimpanzees in feeding upon driver ants

The use of stick tools by wild chimpanzees (Pan troglodytes) to feed upon driver ants (Dorylus (Anomma) nigricans) is described. Observations of this ant dipping were made over five years in the Gombe National Park in western Tanzania. Chimpanzees find the nomadic ant colonies visually, often re-visiting the subterranean nest sites until the ants move on. The nest is opened manually and tools are made from green woody vegetation. The ant dipping sequence is intricate and efficient. The chimpanzee predator uses several positioning strategies to minimise the ants' massed defensive tactics. Average intakes of 17–20 g/feeding session are estimated. It is concluded that ants may constitute a significant chimpanzee dietary component and that the dipping tools and techniques are relatively stereotyped in form.     

Effects of Manual Disability on Feeding Skills in Gorillas and Chimpanzees

Foraging gorillas and chimpanzees employ skilful bimanual techniques to process food plants, and there are wild populations in which 10–20% of individuals have severe hand injuries. We examined the feeding skills of one injured gorilla and two injured chimpanzees, while they dealt with plants for which intact peers employ complex techniques. Feeding efficiency was only slightly compromised in the disabled subjects, and none of them had acquired novel techniques specific to their remaining capacity. Instead, all three subjects used techniques like those of able-bodied individuals, though when several optional methods were available, their balance of preference was different. They adapted the techniques to their disabilities by the flexible substitution of a range of alternative means to achieve each step of the process, including unusual grips, use of one hand instead of two or vice versa, and use of the mouth or a foot. Compensation was at the level of detailed execution rather than overall technique and depended on transferring motor organization to novel effector organs. Our findings have implications for theories of the acquisition of complex manual skills in great apes and for the flexibility of great ape mental skills.