Cross-population variation in usage of a call combination: evidence of signal usage flexibility in wild bonobos.

The arbitrary relationship between signifier and signified is one of the features responsible for language's extreme lability, adaptability, and expressiveness. Understanding this arbitrariness and its emergence is essential in any account of the evolution of language. To shed light on the phylogeny of the phenomenon, comparative data examining the relationship between signal form and function in the communication systems of non-humans is central. Here we report the results of a study on the production and usage the whistle-high hoot call combination (W + HH) from two distant populations of wild bonobos (Pan paniscus): Lui Kotale, DRC, and Kokolopori, DRC. We find that the context in which bonobos produce the W + HHs varies systematically between populations. Our results suggest that variation in W + HH production may represent an example of signal-adjustment optionality, a key component of arbitrariness.

Blood pressure monitoring in zoologically managed bonobos (Pan paniscus).

In response to the growing evidence that hypertension may play a significant role in the development of cardiovascular disease (CVD) in bonobos, the Great Ape Heart Project established a finger blood pressure (BP) monitoring protocol for zoo-housed bonobos. The ability to monitor BP without the use of anesthesia provides more opportunities to detect potential hypertension in its early stages allowing for therapeutic intervention that may slow the progression of CVD. No BP reference ranges exist for bonobos due to the lack of an established protocol, the difficulty of measuring BP in animals, and small sample size of zoo-housed bonobos. By working with all 8 institutions in North America that care for bonobos, it was possible to (1) investigate the feasibility of using finger BP devices, and (2) establish BP trends for male and female bonobos. Data were collected from May 2016 to March 2019. Zoos were asked to train for and collect BP measurements from any bonobos willing to participate, regardless of age, sex, or health status as well as to report on the quality of the training and measurements obtained. At the start of the study, the North American bonobo population consisted of 74 bonobos ages 5 years and older at 8 institutions. All 8 institutions submitted at total of 3656 BP readings from 50 bonobos (n = 23 females, n = 27 males; ages 5-51 years) representing 67.57% of the trainable population ages 5 years and older. Of the readings submitted, 2845 were determined to be good quality, reliable BP readings (77.81% useful BP measurements) for 36 of the 50 adult bonobos submitted for this study (59.01% of the adult population ages 10-51 years) but showed limitations in the protocol for the younger population. BP trend analysis showed significant differences between bonobos that were not on medication versus those treated with cardiac medications, with those on cardiac mediations having significantly higher systolic arterial pressure, diastolic arterial pressure, and mean arterial pressure (p ≤ 0.001 for all comparisons). Systolic BP generally increased over age classes (10-19, 20-29, 30-39, 40+ years).

Oxytocin promotes species-relevant outgroup attention in bonobos and chimpanzees.

Previous research has found that oxytocin (OT) is associated with intergroup behaviour in humans as well as wild chimpanzees, and that exogenous OT affects Pan social attention. The two Pan species, bonobos and chimpanzees, differ drastically from one another in their intensity of intergroup competition, with lethal intergroup aggression often led by males in chimpanzees and more tolerant associations often centered around females in bonobos. However, it remains unclear how exogenous OT changes the two species' responses to ingroup and outgroup individuals. In this study, after intranasal administration of nebulized OT or placebo control, chimpanzees and bonobos viewed image pairs of ingroup and outgroup conspecifics while their eye movements were tracked with an eye-tracker. Although the overall effect of OT was small, we found that OT shifted bonobos' and chimpanzees' attention to outgroup images of the sex primarily involved in intergroup encounters in each species. Specifically, OT selectively shifted attention towards outgroup photos of female conspecifics in bonobos, and those of outgroup male conspecifics in chimpanzees. This suggests that OT generally promotes outgroup attention in both bonobos and chimpanzees but this effect is restricted to the sex most relevant in intergroup relations. These results suggest that, although OT may have a generally conserved role in hominid intergroup behaviour, it may act in species-relevant ways under the influence of their socio-ecological backgrounds.

Testing the effect of oxytocin on social grooming in bonobos.

Oxytocin has attracted research attention due to its role in promoting social bonding. In bonobos and chimpanzees, the two species most closely related to humans, urinary oxytocin is known to correlate with key behaviours related to social bonding such as social grooming in chimpanzees and female-female sexual behaviour in bonobos. However, no study has demonstrated that the administration of oxytocin promotes real-life social interactions in Pan, leaving it unclear whether oxytocin is merely correlated with social behaviors or does affect them in these species. To test this, we administered nebulized oxytocin or saline placebo to a group of female bonobos and subsequently observed changes in their gross behavior during free interaction. We found an overall effect of more frequent grooming in the oxytocin condition. However, on the individual level this effect remained significant for only one participant in our follow-up models, suggesting future work should explore interindividual variation. Our results provide some experimental support for the biobehavioural feedback loop hypothesis, which posits that some functions of the oxytocin system support the formation and maintenance of social bonds through a positive feedback loop; however, further tests with a larger number of individuals are required. Our results, at a minimum, demonstrated that oxytocin affects spontaneous, naturalistic social interactions of at least some female bonobos, adding to accumulating evidence that oxytocin modulates complex social behaviors of Pan.

In vivo deciduous dental eruption in LuiKotale bonobos and Gombe chimpanzees.

OBJECTIVES: Existing data on bonobo and chimpanzee dental eruption timing are derived predominantly from captive individuals or deceased wild individuals. However, recent advances in noninvasive photographic monitoring of living, wild apes have enabled researchers to characterize dental eruption in relatively healthy individuals under naturalistic conditions. At present, such data are available for only one population of wild chimpanzees. We report data for an additional population of wild chimpanzees and the first dental eruption data for wild bonobos. MATERIALS AND METHODS: We collected photographs and video footage of teeth from the open mouths of wild bonobos and East African chimpanzees of known age from LuiKotale, Democratic Republic of the Congo, and Gombe National Park, Tanzania, respectively. We scored the presence and absence of deciduous teeth from photographs and video footage to characterize deciduous dental eruption timing in these two populations. RESULTS: Deciduous dental eruption ages in our sample fall within the range of variation previously documented for captive chimpanzees, but eruption ages are later in wild than in captive contexts. We found substantial variation in deciduous canine eruption timing, particularly among bonobos. One bonobo had a deciduous canine present by 227 days old while another did not have a deciduous canine present at 477 days old. DISCUSSION: Our data indicate that deciduous teeth erupt later in wild individuals than in captive individuals. We also found that deciduous dental eruption timing varies considerably between individuals within our study populations, a pattern that is consistent with previous studies. Future studies should consider sources of variation in deciduous canine eruption timing and relationships with other aspects of life history as additional data become available.

A Test of Foraging Models Using Dietary Diversity Indices for the Lomako Forest Bonobos.

Optimal diet and functional response models are used to understand the evolution of primate foraging strategies. The predictions of these models can be tested by examining the geographic and seasonal variation in dietary diversity. Dietary diversity is a useful tool that allows dietary comparisons across differing sampling locations and time periods. Bonobos (Pan paniscus) are considered primarily frugivorous and consume fruits, leaves, insects, vertebrates, terrestrial herbaceous vegetation, and flowers. Frugivores, like bonobos, are valuable for examining dietary diversity and testing foraging models because they eat a variety of species and are subject to seasonal shifts in fruit availability. Frugivorous primate species thus allow for tests of how variation in dietary diversity is correlated with variation in ecological factors. We investigated measures of dietary diversity in bonobos at two research camps across field seasons within the same protected area (N'dele and Iyema) in Lomako Forest, Democratic Republic of the Congo. We compared the results of behavioral observation (1984/1985, 1991, 1995, 2014, and 2017) and fecal washing analysis (2007 and 2009) between seasons and study period using three diversity indices (Shannon's, Simpson's, and SW evenness). The average yearly dietary diversity indices at N'dele were Shannon's H' = 2.04, Simpson's D = 0.82, and SW evenness = 0.88 while at Iyema, the indices were Shannon's H' = 2.02, Simpson's D = 0.82, and SW evenness = 0.88. Behavioral observation data sets yielded significantly higher dietary diversity indices than fecal washing data sets. We found that food item (fruit, leaf, and flower) consumption was not associated with seasonal food availability for the 2017 behavioral observation data set. Shannon's index was lower during periods when fewer bonobo dietary items were available to consume and higher when fruit was abundant. Finally, we found that optimal diet models best-explained patterns of seasonal food availability and dietary diversity. Dietary diversity is an essential factor to consider when understanding primate diets and can be a tool in understanding variation in primate diets, particularly among frugivores. Dietary diversity varies across populations of the same species and across time, and it is critical in establishing a complete understanding of how primate diets change over time.

Vocal-gestural combinations in infant bonobos: new insights into signal functional specificity.

Comparing the communicative abilities of humans and great apes is a commonly used research strategy to understand the evolutionary foundation of modern human language. The ability to combine signals from different communicative modes (vocal, gestural, facial, etc.) is a universal and important feature of human language that is shared with great apes, although rarely investigated. Research on apes' signal combination has usually studied the frequency, distribution, effectiveness, and function of combinations in comparison with single signals, but only seldom have studies addressed their functional specificity, i.e., their ability to convey specific signallers' goals within contexts. Here, I suggest a new methodological approach to the investigation of functional specificity of signals, which consists of focusing on one call type and exploring its various patterns of production when combined with gestures. I illustrate the different methodological steps with a case study on infant bonobos' combinations of 'Pout moan' calls with gestures in the context of infant-to-mother requests. The descriptive results indicate that at least three combinations seem functionally specific, i.e., specific to the infants' desired goals. It suggests that combinations can be functionally specific from a young age and that learning how to combine signals efficiently might occur early in ontogeny. This suggested approach might provide insight to the on-going debate regarding the mechanisms underpinning the learning process of successful signal production and potentially further our understanding of the evolution of the combinatorial characteristics of human communication.

Epiphyseal fusion and dental development in Pan paniscus with comparisons with Pan troglodytes.

OBJECTIVES: Compared with frequent studies of skeletal development in chimpanzees, relatively little is known about bonobo skeletal development. This study seeks to explore the relationship between skeletal and dental development in both species of Pan. New data are presented for fusion sites not previously observed in bonobos. MATERIALS AND METHODS: In a sample of 34 Pan paniscus and 168 Pan troglodytes subadults, state of fusion was recorded for 30 epiphyseal fusion sites using a three-stage system of unfused, midfusion, and complete fusion based on Wintheiser, Clauser, and Tappen. Stage of dental development for permanent mandibular dentition was assessed using the Demrijian, Goldstein, and Tanner method. These data allowed for comparisons of both species of Pan and the two subspecies of P. troglodytes. RESULTS: The sequence of fusion events was generally consistent between the two species, but some exceptions may exist for the knee and ankle. The number of fusion events that occurred after complete dental mineralization was similar in both species. No statistically significant differences were found in the fusion timing for the subspecies of P. troglodytes. DISCUSSION: Bolter and Zihlman suggested that fusion at the acetabulum occurs earlier in Pan paniscus, while fusion of epiphyses at the knee are delayed, compared with P. troglodytes. Our data do not indicate earlier fusion of the acetabulum, but fusion events at the knee may complete later relative to dental mineralization in Pan pansicus. Compared with Homo sapiens, both P. troglodytes and Pan paniscus demonstrate later completion of epiphyseal fusion relative to dental mineralization.

Chimpanzees, bonobos and children successfully coordinate in conflict situations.

Social animals need to coordinate with others to reap the benefits of group-living even when individuals' interests are misaligned. We compare how chimpanzees, bonobos and children coordinate their actions with a conspecific in a Snowdrift game, which provides a model for understanding how organisms coordinate and make decisions under conflict. In study 1, we presented pairs of chimpanzees, bonobos and children with an unequal reward distribution. In the critical condition, the preferred reward could only be obtained by waiting for the partner to act, with the risk that if no one acted, both would lose the rewards. Apes and children successfully coordinated to obtain the rewards. Children used a 'both-partner-pull' strategy and communicated during the task, while some apes relied on an 'only-one-partner-pulls' strategy to solve the task, although there were also signs of strategic behaviour as they waited for their partner to pull when that strategy led to the preferred reward. In study 2, we presented pairs of chimpanzees and bonobos with the same set-up as in study 1 with the addition of a non-social option that provided them with a secure reward. In this situation, apes had to actively decide between the unequal distribution and the alternative. In this set-up, apes maximized their rewards by taking their partners' potential actions into account. In conclusion, children and apes showed clear instances of strategic decision-making to maximize their own rewards while maintaining successful coordination.

The stable isotope ecology of Pan in Uganda and beyond.

Stable isotope analysis has long been used to study the dietary ecology of living and fossil primates, and there has been increasing interest in using stable isotopes to study primate habitat use and anthropogenic impacts on non-human primates. Here, we examine the stable carbon and nitrogen isotope compositions of chimpanzees (Pan troglodytes) from seven communities in Uganda across a continuum of habitat structure (closed to more open) and access to anthropogenic resources (no reliance to heavy reliance). In general, the hair δ(13) C, but not δ(15) N, values of these communities vary depending on forest structure and degree of anthropogenic influence. When integrated with previously published hair δ(13) C and δ(15) N values for Pan, it is apparent that modern "savanna" and "forest" Pan form discrete clusters in carbon and nitrogen isotope space, although there are exceptions probably relating to microhabitat specialization. The combined dataset also reveals that Pan δ(13) C values (but not δ(15) N values) are inversely related to rainfall (r(2) = 0.62). We converted Pan hair δ(13) C values to enamel equivalents and made comparisons to the fossil hominoids Sivapithecus sp., Gigantopithecus blacki, Ardipithecus ramidus, and Australopithecus anamensis. The δ(13) C values of the fossil hominins Ar. ramidus and Au. anamensis do not cluster with the δ(13) C values of modern Pan in "forest" habitats, or with fossil hominoids that are believed to have inhabited forests. Am. J. Primatol. 78:1070-1085, 2016. © 2016 Wiley Periodicals, Inc.

Habituating field scientists.

This article explores the sensory dimensions of scientific field research in the only region in the world where free-ranging bonobos ( Pan paniscus) can be studied in their natural environment; the equatorial rainforest of the Democratic Republic of Congo. If, as sensory anthropologists have argued, the senses are developed, grown and honed in a given cultural and environmental milieu, how is it that field scientists come to dwell among familiarity in a world which is, at first, unfamiliar? This article builds upon previous anthropological and philosophical engagements with habituation that have critically examined primatologists' attempts to become 'neutral objects in the environment' in order to habituate wild apes to their presence. It does so by tracing the somatic modes of attention developed by European and North American researchers as they follow bonobos in these forests. The argument is that as environments, beings and their elements become familiar, they do not become 'neutral', but rather, suffused with meaning.

Body language: The interplay between positional behavior and gestural signaling in the genus Pan and its implications for language evolution.

OBJECTIVES: The gestural repertoires of bonobos and chimpanzees are well documented, but the relationship between gestural signaling and positional behavior (i.e., body postures and locomotion) has yet to be explored. Given that one theory for language evolution attributes the emergence of increased gestural communication to habitual bipedality, this relationship is important to investigate. MATERIALS AND METHODS: In this study, we examined the interplay between gestures, body postures, and locomotion in four captive groups of bonobos and chimpanzees using ad libitum and focal video data. RESULTS: We recorded 43 distinct manual (involving upper limbs and/or hands) and bodily (involving postures, locomotion, head, lower limbs, or feet) gestures. In both species, actors used manual and bodily gestures significantly more when recipients were attentive to them, suggesting these movements are intentionally communicative. Adults of both species spent less than 1.0% of their observation time in bipedal postures or locomotion, yet 14.0% of all bonobo gestures and 14.7% of all chimpanzee gestures were produced when subjects were engaged in bipedal postures or locomotion. Among both bonobo groups and one chimpanzee group, these were mainly manual gestures produced by infants and juvenile females. Among the other chimpanzee group, however, these were mainly bodily gestures produced by adult males in which bipedal posture and locomotion were incorporated into communicative displays. DISCUSSION: Overall, our findings reveal that bipedality did not prompt an increase in manual gesturing in these study groups. Rather, body postures and locomotion are intimately tied to many gestures and certain modes of locomotion can be used as gestures themselves.

Feeding ecology of bonobos living in forest-savannah mosaics: Diet seasonal variation and importance of fallback foods.

Primates along with many other animal taxa are forced to cope with large shifts in basic ecological conditions because of rapid anthropogenically induced changes of their habitats. One of the coping strategies for primates is to adjust their diet to these changes, and several studies have demonstrated the importance of fallback resources for this. Bonobos, like chimpanzees, might be particularly vulnerable to habitat fragmentation because of their high dependence on fruit availability. Little is known, however, about bonobo feeding ecology in fragmented habitats and their use of fallback resources. In this study, we investigate diet seasonal variation and the exploitation of preferred and fallback foods in a bonobo population living in forest-savannah mosaics. Results show that bonobos have adapted to this fragmented habitat by feeding on only a few fruit species, including an important number of non-tree species (liana, herb and savannah shrub), in comparison to populations living in dense forests. These non-tree plants have been defined as fallback and non-preferred foods, which are most probably consumed to maintain high frugivory. Interestingly, we identified that preferred foods are all typical of mature forests while fallback resources are mainly found in forest edges or disturbed areas. This finding indicates that bonobos prefer to use mature forests when feeding, as they do for nesting, but extend their range use to forest areas in close proximity to humans when the availability of preferred fruits is low. Finally, we show that bonobo diet relies heavily on two abundant fallback fruits: Musanga cecropioides and Marantochloa leucantha. Other studies have demonstrated that the selection of abundant fallback resources enables primates to subsist at high densities and to maintain cohesive groups, as observed at this study site. Our findings suggest that bonobos living in forest-savannah mosaics can be considered as staple fallback food consumers. Am. J. Primatol. 77:948-962, 2015. © 2015 Wiley Periodicals, Inc.

Differences in the early cognitive development of children and great apes.

There is very little research comparing great ape and human cognition developmentally. In the current studies we compared a cross-sectional sample of 2- to 4-year-old human children (n=48) with a large sample of chimpanzees and bonobos in the same age range (n=42, hereafter: apes) on a broad array of cognitive tasks. We then followed a group of juvenile apes (n=44) longitudinally over 3 years to track their cognitive development in greater detail. In skills of physical cognition (space, causality, quantities), children and apes performed comparably at 2 years of age, but by 4 years of age children were more advanced (whereas apes stayed at their 2-year-old performance levels). In skills of social cognition (communication, social learning, theory of mind), children out-performed apes already at 2 years, and increased this difference even more by 4 years. Patterns of development differed more between children and apes in the social domain than the physical domain, with support for these patterns present in both the cross-sectional and longitudinal ape data sets. These results indicate key differences in the pattern and pace of cognitive development between humans and other apes, particularly in the early emergence of specific social cognitive capacities in humans.

Dynamic inconsistency in great apes.

When presented with the option of either an immediate benefit or a larger, later reward, we may behave impatiently by choosing instant gratification. Nonetheless, when we can make the same decision ahead of time and plan for the future, we tend to make more patient choices. Here, we explored whether great apes share this core feature of human decision-making, often referred to as dynamic inconsistency. We found that orangutans, bonobos, and gorillas tended to act impatiently and with considerable variability between individuals when choosing between an immediate reward and a larger-later reward, which is a commonly employed testing method in the field. However, with the inclusion of a front-end delay for both alternatives, their decisions became more patient and homogeneous. These results show that great apes are dynamically inconsistent. They also suggest that, when choosing between future outcomes, they are more patient than previously reported. We advocate for the inclusion of diverse time ranges in comparative research, especially considering the intertwinement of intertemporal choices and future-oriented behavior.

Does tolerance allow bonobos to outperform chimpanzees on a cooperative task? A conceptual replication of Hare et al., 2007.

Across various taxa, social tolerance is thought to facilitate cooperation, and many species are treated as having species-specific patterns of social tolerance. Yet studies that assess wild and captive bonobos and chimpanzees result in contrasting findings. By replicating a cornerstone experimental study on tolerance and cooperation in bonobos and chimpanzees (Hare et al. 2007 Cur. Biol. 17, 619-623 (doi:10.1016/j.cub.2007.02.040)), we aim to further our understanding of current discrepant findings. We tested bonobos and chimpanzees housed at the same facility in a co-feeding and cooperation task. Food was placed on dishes located on both ends or in the middle of a platform. In the co-feeding task, the tray was simply made available to the ape duos, whereas in the cooperation task the apes had to simultaneously pull at both ends of a rope attached to the platform to retrieve the food. By contrast to the published findings, bonobos and chimpanzees co-fed to a similar degree, indicating a similar level of tolerance. However, bonobos cooperated more than chimpanzees when the food was monopolizable, which replicates the original study. Our findings call into question the interpretation that at the species level bonobos cooperate to a higher degree because they are inherently more tolerant.

Attention Towards Pupil Size in Humans and Bonobos (Pan paniscus).

Previous work has established that humans have an attentional bias towards emotional signals, and there is some evidence that this phenomenon is shared with bonobos, our closest relatives. Although many emotional signals are explicit and overt, implicit cues such as pupil size also contain emotional information for observers. Pupil size can impact social judgment and foster trust and social support, and is automatically mimicked, suggesting a communicative role. While an attentional bias towards more obvious emotional expressions has been shown, it is unclear whether this also extends to a more subtle implicit cue, like changes in pupil size. Therefore, the current study investigated whether attention is biased towards pupils of differing sizes in humans and bonobos. A total of 150 human participants (141 female), with a mean age of 19.13 (ranging from 18 to 32 years old), completed an online dot-probe task. Four female bonobos (6 to 17 years old) completed the dot-probe task presented via a touch screen. We used linear mixed multilevel models to examine the effect of pupil size on reaction times. In humans, our analysis showed a small but significant attentional bias towards dilated pupils compared to intermediate-sized pupils and intermediate-sized pupils when compared to small pupils. Our analysis did not show a significant effect in bonobos. These results suggest that the attentional bias towards emotions in humans can be extended to a subtle unconsciously produced signal, namely changes in pupil size. Due to methodological differences between the two experiments, more research is needed before drawing a conclusion regarding bonobos. Supplementary Information: The online version contains supplementary material available at 10.1007/s42761-022-00146-1.

Prevalence of antibodies against human respiratory viruses potentially involving anthropozoonoses in wild bonobos.

One of the current threats to the bonobo (Pan paniscus), a highly endangered ape species only found in the Democratic Republic of the Congo, are anthropozoonoses caused by human respiratory viruses. To date, epidemiological information regarding respiratory viral infections in bonobos is limited. In this study, we examined fecal immunoglobulin A antibodies against human respiratory viruses in bonobos, which may help estimating the viral prevalence. A substantial proportion of bonobos were positive for the antiviral antibodies, including those against parainfluenza virus, respiratory syncytial virus, influenza virus, rhinovirus, and mumps virus. The prevalence of the antibodies was found to depend on the viral species and bonobo populations, suggesting that the bonobos had been exposed to these respiratory viruses. These results may indicate the need for an epidemiological evidence-based action plan for the protection of bonobos from anthropozoonoses.

Targeted helping and cooperation in zoo-living chimpanzees and bonobos.

Directly comparing the prosocial behaviour of our two closest living relatives, bonobos and chimpanzees, is essential to deepening our understanding of the evolution of human prosociality. We examined whether helpers of six dyads of chimpanzees and bonobos transferred tools to a conspecific. In the experiment 'Helping', transferring a tool did not benefit the helper, while in the experiment 'Cooperation', the helper only obtained a reward by transferring the correct tool. Chimpanzees did not share tools with conspecifics in either experiment, except for a mother-daughter pair, where the mother shared a tool twice in the experiment 'Helping'. By contrast, all female-female bonobo dyads sometimes transferred a tool even without benefit. When helpers received an incentive, we found consistent transfers in all female-female bonobo dyads but none in male-female dyads. Even though reaching by the bonobo receivers increased the likelihood that a transfer occurred, we found no significant species difference in whether receivers reached to obtain tools. Thus, receivers' behaviour did not explain the lack of transfers from chimpanzee helpers. This study supports the notion that bonobos might have a greater ability to understand social problems and the collaborative nature of such tasks.