Bonobos extract meaning from call sequences

Studies on language-trained bonobos have revealed their remarkable abilities in representational and communication tasks. Surprisingly, however, corresponding research into their natural communication has largely been neglected. We address this issue with a first playback study on the natural vocal behaviour of bonobos. Bonobos produce five acoustically distinct call types when finding food, which they regularly mix together into longer call sequences. We found that individual call types were relatively poor indicators of food quality, while context specificity was much greater at the call sequence level. We therefore investigated whether receivers could extract meaning about the quality of food encountered by the caller by integrating across different call sequences. We first trained four captive individuals to find two types of foods, kiwi (preferred) and apples (less preferred) at two different locations. We then conducted naturalistic playback experiments during which we broadcasted sequences of four calls, originally produced by a familiar individual responding to either kiwi or apples. All sequences contained the same number of calls but varied in the composition of call types. Following playbacks, we found that subjects devoted significantly more search effort to the field indicated by the call sequence. Rather than attending to individual calls, bonobos attended to the entire sequences to make inferences about the food encountered by a caller. These results provide the first empirical evidence that bonobos are able to extract information about external events by attending to vocal sequences of other individuals and highlight the importance of call combinations in their natural communication system.     

Nonconceptive Sexual Behavior in Bonobos and Capuchins

Sexual behavior by infecundable females, and by same-sex and adult-immature dyads, occurs in wild and captive bonobos (Pan paniscus). Proposed functions of these behaviors, in social primates generally, include practice, paternity confusion, exchange, and communication as well as appeasement. We used this framework to interpret and to compare observations of sexual behavior in a captive bonobo group and a wild white-faced capuchin (Cebus capucinus) group. In both species, (a) sexual behavior was no more frequent in cycling females than in pregnant or lactating females and (b) same-sex and adult-immature dyads engaged in as much mounting or genitogenital contact as adult heterosexual dyads did. The species differed in that (a) bonobos engaged in sexual behavior 65 times as frequently as capuchins, (b) only bonobos engaged in sexual contact other than ventrodorsal mounting during focal observation, and (c) bonobo sexual contact was concentrated most heavily in socially tense situations in adult female–female dyads, whereas capuchin sexual contact was concentrated most heavily in socially tense situations in adult male–male dyads. These data and published literature indicate that (a) practice sex occurs in both species, (b) paternity confusion may be a current function of C. capucinus nonconceptive sex, (c) exchange sex remains undemonstrated in capuchins, and (d) communication sex is more important to members of the transferring sex—female bonobos and male capuchins—than to members of the philopatric sex.     

Bonobos Protect and Console Friends and Kin

Post-conflict third-party affiliation has been reported to have different functional meanings, one of them being consolation. Here, we tested the main hypotheses that have been put forth to explain the presence of this phenomenon at a functional level in the bonobo: Self-Protection Hypothesis, Victim-Protection Hypothesis, Relationship-Repair or Substitute for Reconciliation Hypothesis, and Consolation Hypothesis. By analyzing the data collected over 10 years, we investigated what factors affected the distribution of both spontaneous third party affiliation (initiated by the bystander) and solicited third party affiliation (initiated by the victim). We considered factors related to the individual features (sex, rank, age) of victim and bystander, their relationship quality (kinship, affiliation), and the effect that third party affiliation had on the victim (such as protection against further attacks and anxiety reduction). Both spontaneous and solicited third party affiliation reduced the probability of further aggression by group members on the victim (Victim-Protection Hypothesis supported). Yet, only spontaneous affiliation reduced victim anxiety (measured via self-scratching), thus suggesting that the spontaneous gesture – more than the protection itself – works in calming the distressed subject. The victim may perceive the motivational autonomy of the bystander, who does not require an invitation to provide post-conflict affiliative contact. Moreover, spontaneous - but not solicited - third party affiliation was affected by the bond between consoler and victim, being the relationship between consoler and aggressor irrelevant to the phenomenon distribution (Consolation Hypothesis supported). Spontaneous affiliation followed the empathic gradient described for humans, being mostly offered to kin, then friends, then acquaintances. Overall, our findings do not only indicate the consolatory function of spontaneous third-party affiliation but they also suggest that consolation in the bonobo may be an empathy-based phenomenon.     

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.     

Bonobos fall within the genomic variation of chimpanzees

To gain insight into the patterns of genetic variation and evolutionary relationships within and between bonobos and chimpanzees, we sequenced 150,000 base pairs of nuclear DNA divided among 15 autosomal regions as well as the complete mitochondrial genomes from 20 bonobos and 58 chimpanzees. Except for western chimpanzees, we found poor genetic separation of chimpanzees based on sample locality. In contrast, bonobos consistently cluster together but fall as a group within the variation of chimpanzees for many of the regions. Thus, while chimpanzees retain genomic variation that predates bonobo-chimpanzee speciation, extensive lineage sorting has occurred within bonobos such that much of their genome traces its ancestry back to a single common ancestor that postdates their origin as a group separate from chimpanzees.     

Multi-Modal Use of a Socially Directed Call in Bonobos

‘Contest hoots’ are acoustically complex vocalisations produced by adult and subadult male bonobos (Pan paniscus). These calls are often directed at specific individuals and regularly combined with gestures and other body signals. The aim of our study was to describe the multi-modal use of this call type and to clarify its communicative and social function. To this end, we observed two large groups of bonobos, which generated a sample of 585 communicative interactions initiated by 10 different males. We found that contest hooting, with or without other associated signals, was produced to challenge and provoke a social reaction in the targeted individual, usually agonistic chase. Interestingly, ‘contest hoots’ were sometimes also used during friendly play. In both contexts, males were highly selective in whom they targeted by preferentially choosing individuals of equal or higher social rank, suggesting that the calls functioned to assert social status. Multi-modal sequences were not more successful in eliciting reactions than contest hoots given alone, but we found a significant difference in the choice of associated gestures between playful and agonistic contexts. During friendly play, contest hoots were significantly more often combined with soft than rough gestures compared to agonistic challenges, while the calls'' acoustic structure remained the same. We conclude that contest hoots indicate the signaller''s intention to interact socially with important group members, while the gestures provide additional cues concerning the nature of the desired interaction.     

Differences in the Cognitive Skills of Bonobos and Chimpanzees

While bonobos and chimpanzees are both genetically and behaviorally very similar, they also differ in significant ways. Bonobos are more cautious and socially tolerant while chimpanzees are more dependent on extractive foraging, which requires tools. The similarities suggest the two species should be cognitively similar while the behavioral differences predict where the two species should differ cognitively. We compared both species on a wide range of cognitive problems testing their understanding of the physical and social world. Bonobos were more skilled at solving tasks related to theory of mind or an understanding of social causality, while chimpanzees were more skilled at tasks requiring the use of tools and an understanding of physical causality. These species differences support the role of ecological and socio-ecological pressures in shaping cognitive skills over relatively short periods of evolutionary time.     

Effects of Epidemic Diseases on the Distribution of Bonobos

This study examined how outbreaks and the occurrence of Anthrax, Ebola, Monkeypox and Trypanosomiasis may differentially affect the distribution of bonobos (Pan paniscus). Using a combination of mapping, Jaccard overlapping coefficients and binary regressions, the study determined how each disease correlated with the extent of occurrence of, and the areas occupied by, bonobos. Anthrax has only been reported to occur outside the range of bonobos and so was not considered further. Ebola, Monkeypox and Trypanosomiasis were each reported within the area of occupancy of bonobos. Their respective overlap coefficients were: J = 0.10; Q_{α = 0.05} = 2.00 (odds ratios = 0.0001, 95% CI = 0.0057; Z = −19.41, significant) for Ebola; J = 1.00; Q_{α = 0.05} = 24.0 (odds ratios = 1.504, 95% CI = 0.5066–2.6122) for Monkeypox; and, J = 0.33; Q_{α = 0.05} = 11.5 (Z = 1.14, significant) for Trypanosomiasis. There were significant relationships for the presence and absence of Monkeypox and Trypanosomiasis and the known extent of occurrence of bonobos, based on the equations y = 0.2368Ln(x)+0.8006 (R² = 0.9772) and y = −0.2942Ln(x)+0.7155 (R² = 0.698), respectively. The positive relationship suggested that bonobos tolerated the presence of Monkeypox. In contrast, the significant negative coefficient suggested that bonobos were absent in areas where Trypanosomiasis is endemic. Our results suggest that large rivers may have prevented Ebola from spreading into the range of bonobos. Meanwhile, Trypanosomiasis has been recorded among humans within the area of occurrence of bonobos, and appears the most important disease in shaping the area of occupancy of bonobos within their overall extent of occupancy.     

Dogs' Social Referencing towards Owners and Strangers

Social referencing is a process whereby an individual uses the emotional information provided by an informant about a novel object/stimulus to guide his/her own future behaviour towards it. In this study adult dogs were tested in a social referencing paradigm involving a potentially scary object with either their owner or a stranger acting as the informant and delivering either a positive or negative emotional message. The aim was to evaluate the influence of the informant''s identity on the dogs'' referential looking behaviour and behavioural regulation when the message was delivered using only vocal and facial emotional expressions. Results show that most dogs looked referentially at the informant, regardless of his/her identity. Furthermore, when the owner acted as the informant dogs that received a positive emotional message changed their behaviour, looking at him/her more often and spending more time approaching the object and close to it; conversely, dogs that were given a negative message took longer to approach the object and to interact with it. Fewer differences in the dog''s behaviour emerged when the informant was the stranger, suggesting that the dog-informant relationship may influence the dog''s behavioural regulation. Results are discussed in relation to studies on human-dog communication, attachment, mood modification and joint attention.     

In Bonobos Yawn Contagion Is Higher among Kin and Friends

In humans, the distribution of yawn contagion is shaped by social closeness with strongly bonded pairs showing higher levels of contagion than weakly bonded pairs. This ethological finding led the authors to hypothesize that the phenomenon of yawn contagion may be the result of certain empathic abilities, although in their most basal form. Here, for the first time, we show the capacity of bonobos (Pan paniscus) to respond to yawns of conspecifics. Bonobos spontaneously yawned more frequently during resting/relaxing compared to social tension periods. The results show that yawn contagion was context independent suggesting that the probability of yawning after observing others'' yawns is not affected by the propensity to engage in spontaneous yawns. As it occurs in humans, in bonobos the yawing response mostly occurred within the first minute after the perception of the stimulus. Finally, via a Linear Mixed Model we tested the effect of different variables (e.g., sex, rank, relationship quality) on yawn contagion, which increased when subjects were strongly bonded and when the triggering subject was a female. The importance of social bonding in shaping yawn contagion in bonobos, as it occurs in humans, is consistent with the hypothesis that empathy may play a role in the modulation of this phenomenon in both species. The higher frequency of yawn contagion in presence of a female as a triggering subject supports the hypothesis that adult females not only represent the relational and decisional nucleus of the bonobo society, but also that they play a key role in affecting the emotional states of others.     

Chromatin Proteins Share Antigenic Determinants with Neurofilaments

Antigenic determinants common to distinct proteins may be unambiguously identified by the use of monoclonal antibodies. Some monoclonal antibodies to mammalian neurofilaments have recently been shown to cross-react with the neurofibrillary tangles found at high density in the brains of senile dements with Alzheimers disease (SDAT). Here, we show that these antibodies also cross-react with chromatin proteins, including the linker histones H1 and H1(0). Elevated levels of histone H1(0) have also been reported in SDAT brains.     

A Comparison Between Bonobos and Chimpanzees: A Review and Update

Chimpanzees (Pan troglodytes) and bonobos (P. paniscus) are our closest living relatives, with the human lineage diverging from the Pan lineage only around five to seven Mya, but possibly as early as eight Mya.^1–2 Chimpanzees and bonobos even share genetic similarities with humans that they do not share with each other.² Given their close genetic relationship to humans, both Pan species represent crucial living models for reconstructing our last common ancestor (LCA) and identifying uniquely human features. Comparing the similarities and differences of the two Pan is thus essential for constructing balanced models of human evolution.³