Selective deforestation and exposure of African wildlife to bat-borne viruses.

Proposed mechanisms of zoonotic virus spillover often posit that wildlife transmission and amplification precede human outbreaks. Between 2006 and 2012, the palm Raphia farinifera, a rich source of dietary minerals for wildlife, was nearly extirpated from Budongo Forest, Uganda. Since then, chimpanzees, black-and-white colobus, and red duiker were observed feeding on bat guano, a behavior not previously observed. Here we show that guano consumption may be a response to dietary mineral scarcity and may expose wildlife to bat-borne viruses. Videos from 2017-2019 recorded 839 instances of guano consumption by the aforementioned species. Nutritional analysis of the guano revealed high concentrations of sodium, potassium, magnesium and phosphorus. Metagenomic analyses of the guano identified 27 eukaryotic viruses, including a novel betacoronavirus. Our findings illustrate how "upstream" drivers such as socioeconomics and resource extraction can initiate elaborate chains of causation, ultimately increasing virus spillover risk.

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees.

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

Chimpanzee pant-hoots encode individual information more reliably than group differences.

Vocal learning, the ability to modify the acoustic structure of vocalizations based on social experience, is a fundamental feature of speech in humans (Homo sapiens). While vocal learning is common in taxa such as songbirds and whales, the vocal learning capacities of nonhuman primates appear more limited. Intriguingly, evidence for vocal learning has been reported in chimpanzees (Pan troglodytes), for example, in the form of regional variation ("dialects") in the "pant-hoot" calls. This suggests that some capacity for vocal learning may be an ancient feature of the Pan-Homo clade. Nonetheless, reported differences have been subtle, with intercommunity variation representing only a small portion of the total acoustic variation. To gain further insights into the extent of regional variation in chimpanzee vocalizations, we performed an analysis of pant-hoots from chimpanzees in the neighboring Kasekela and Mitumba communities at Gombe National Park, Tanzania, and the geographically distant Kanyawara community at Kibale National Park, Uganda. We did not find any statistically significant differences between the neighboring communities at Gombe or among geographically distant communities. Furthermore, we found differences among individuals in all communities. Hence, the variation in chimpanzee pant-hoots reflected individual differences, rather than group differences. Thus, we did not find evidence of dialects in this population, suggesting that extensive vocal learning emerged only after the lineages of Homo and Pan diverged.

The effect of warning signs on the presence of snare traps in a Ugandan rainforest.

Since chimpanzee (Pan troglodytes) conservation often involves local human populations, conservation strategies must consider psychological factors that impact their behavior. In Budongo Forest, Uganda, for example, local communities commonly engage in snare trap (hereafter: snare) setting for wild meat. This illegal activity posits a substantial threat to wild chimpanzees, causing permanent wounds or death for those who are snared. Despite various schemes previously implemented to address snare setting-an activity that is fueled by poverty, the problem and its detrimental impact on chimpanzees persists. Here, we experimentally tested a novel intervention, a systematic display of specially designed warning signs aimed at local poachers. We monitored the presence of snares before and after introducing these signs over a total period of two years and compared it with that of a similar sized control area with no intervention. Results show that snares were less likely to be present during the "sign" period than during the "non-sign" period in the experimental but not in the control area. We discuss the potential of this cost-effective intervention for limiting illegal activities that pose a severe threat to chimpanzees and other species inhabiting tropical forests.

Dead-infant carrying by chimpanzee mothers in the Budongo Forest.

It has been suggested that non-human primates can respond to deceased conspecifics in ways that suggest they experience psychological states not unlike humans, some of which could indicate they exhibit a notion of death. Here, we report long-term demographic data from two East African chimpanzee groups. During a combined 40-year observation period, we recorded 191 births of which 68 died in infancy, mostly within the first year. We documented the post-mortem behaviour of the mothers and describe nine occasions where Budongo chimpanzee mothers carried infants for 1-3 days after their death, usually until the body started to decompose. We also observed three additional cases of extended carrying lasting for more than 2 weeks, one of which was followed by the unusual extended carrying of an object and another which lasted 3 months. In each case, the corpses mummified. In addition, we report four instances of recurring dead-infant carrying by mothers, three of whom carried the corpse for longer during the second instance. We discuss these observations in view of functional hypotheses of dead-infant carrying in primates and the potential proximate mechanisms involved in this behaviour.

First observation of a chimpanzee with albinism in the wild: Social interactions and subsequent infanticide.

Albinism-the congenital absence of pigmentation-is a very rare phenomenon in animals due to the significant costs to fitness of this condition. Both humans and non-human individuals with albinism face a number of challenges, such as reduced vision, increased exposure to ultraviolet radiation, or compromised crypticity resulting in an elevated vulnerability to predation. However, while observations of social interactions involving individuals with albinism have been observed in wild non-primate animals, such interactions have not been described in detail in non-human primates (hereafter, primates). Here, we report, to our knowledge, the first sighting of an infant with albinism in wild chimpanzees (Pan troglodytes schweinfurthii), including social interactions between the infant, its mother, and group members. We also describe the subsequent killing of the infant by conspecifics as well as their behavior towards the corpse following the infanticide. Finally, we discuss our observations in relation to our understanding of chimpanzee behavior or attitudes towards individuals with very conspicuous appearances.

Early maternal loss leads to short- but not long-term effects on diurnal cortisol slopes in wild chimpanzees.

The biological embedding model (BEM) suggests that fitness costs of maternal loss arise when early-life experience embeds long-term alterations to hypothalamic-pituitary-adrenal (HPA) axis activity. Alternatively, the adaptive calibration model (ACM) regards physiological changes during ontogeny as short-term adaptations. Both models have been tested in humans but rarely in wild, long-lived animals. We assessed whether, as in humans, maternal loss had short- and long-term impacts on orphan wild chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, both indicative of HPA axis functioning. Immature chimpanzees recently orphaned and/or orphaned early in life had diurnal cortisol slopes reflecting heightened activation of the HPA axis. However, these effects appeared short-term, with no consistent differences between orphan and non-orphan cortisol profiles in mature males, suggesting stronger support for the ACM than the BEM in wild chimpanzees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species.

Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos.

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.

Shifts in Female Facial Attractiveness during Pregnancy.

It has been proposed that women's physical attractiveness is a cue to temporal changes in fertility. If this is the case, we should observe shifts in attractiveness during pregnancy-a unique physiological state of temporal infertility. The aim of this study was to examine how women's facial attractiveness changes during the subsequent trimesters of pregnancy and how it compares to that of nonpregnant women. Sixty-six pictures of pregnant women (22 pictures per trimester) and 22 of nonpregnant women (a control group) were used to generate four composite portraits, which were subsequently assessed for facial attractiveness by 117 heterosexual men. The results show considerable differences between facial attractiveness ratings depending on the status and progress of pregnancy. Nonpregnant women were perceived as the most attractive, and the attractiveness scores of pregnant women decreased throughout the course of pregnancy. Our findings show that facial attractiveness can be influenced by pregnancy and that gestation, even at its early stages, affects facial attractiveness. Considerable changes in women's physiology that occur during pregnancy may be responsible for the observed effects.

The relationship between food calling and agonistic behaviour in wild chimpanzees.

A number of social animals produce food-associated calls, which have been interpreted as informative and referential about the quality or quantity of food accessed by the caller. In chimpanzees, however, some behavioural patterns have remained unexplained by this model, suggesting that food-associated calls have a more generalized social function beyond attracting others to food, such as promoting tolerance between co-feeding individuals. In this study, we investigated how wild chimpanzees (Pan troglodytes schweinfurthii) of Budongo Forest, Uganda, use food associated-calls in situations when social tolerance is low, i.e., during agonistic interactions. We found a positive relationship between food calling and agonistic behaviours during a feeding event, independent of the number of males on the feeding patch. Moreover, food calling followed rather than preceded agonistic interactions, suggesting that aggression can trigger food call production. These results support the view that chimpanzee food-associated calls can act as social tools mediating competitive or aggressive interactions.

Maternal cannibalism in two populations of wild chimpanzees.

Maternal cannibalism has been reported in several animal taxa, prompting speculations that the behavior may be part of an evolved strategy. In chimpanzees, however, maternal cannibalism has been conspicuously absent, despite high levels of infant mortality and reports of non-maternal cannibalism. The typical response of chimpanzee mothers is to abandon their deceased infant, sometimes after prolonged periods of carrying and grooming the corpse. Here, we report two anomalous observations of maternal cannibalism in communities of wild chimpanzees in Uganda and Ivory Coast and discuss the evolutionary implications. Both infants likely died under different circumstances; one apparently as a result of premature birth, the other possibly as a result of infanticide. In both cases, the mothers consumed parts of the corpse and participated in meat sharing with other group members. Neither female presented any apparent signs of ill health before or after the events. We concluded that, in both cases, cannibalizing the infant was unlikely due to health-related issues by the mothers. We discuss these observations against a background of chimpanzee mothers consistently refraining from maternal cannibalism, despite ample opportunities and nutritional advantages. We conclude that maternal cannibalism is extremely rare in this primate, likely due to early and strong mother-offspring bond formation, which may have been profoundly disrupted in the current cases.

Behavioural patterns of vocal greeting production in four primate species.

Social animals have evolved a range of signals to avoid aggressive and facilitate affiliative interactions. Vocal behaviour is especially important in this respect with many species, including various primates, producing acoustically distinct 'greeting calls' when two individuals approach each other. While the ultimate function of greeting calls has been explored in several species, little effort has been made to understand the mechanisms of this behaviour across species. The aim of this study was to explore how differences in individual features (individual dominance rank), dyadic relationships (dominance distance and social bond strength) and audience composition (presence of high-ranking or strongly bonded individuals in proximity), related to vocal greeting production during approaches between two individuals in the philopatric sex of four primate species: female olive baboons (Papio anubis), male chimpanzees (Pan troglodytes), female sooty mangabeys (Cercocebus atys) and female vervet monkeys (Chlorocebus pygerythrus). We found that female vervet monkeys did not produce greeting calls, while in the other three species, low-ranking individuals were more likely to call than high-ranking ones. The effects of dyadic dominance relationships differed in species-specific ways, with calling being positively associated with the rank distance between two individuals in baboons and chimpanzees, but negatively in mangabeys. In none of the tested species did we find strong evidence for an effect of dyadic affiliative relationships or audience on call production. These results likely reflect deeper evolutionary layers of species-specific peculiarities in social style. We conclude that a comparative approach to investigate vocal behaviour has the potential to not only better understand the mechanisms mediating social signal production but also to shed light on their evolutionary trajectories.

Trade-offs in the production of animal vocal sequences: insights from the structure of wild chimpanzee pant hoots.

BACKGROUND: Vocal sequences - utterances consisting of calls produced in close succession - are common phenomena in animal communication. While many studies have explored the adaptive benefits of producing such sequences, very little is known about how the costs and constraints involved in their production affect their form. Here, we investigated this issue in the chimpanzee (Pan troglodytes schweinfurthii) pant hoot, a long and structurally complex vocal sequence comprising four acoustically distinct phases - introduction, build-up, climax and let-down. RESULTS: We found that in each of these phases, and for the sequence as a whole, there was a negative relationship between the number of calls produced and their average duration. There was also a negative relationship between the total duration of some adjacent phases. Significant relationships between the fundamental frequency of calls and their number or duration were found for some phases of the sequence, but the direction of these relationships differed between particular phases. CONCLUSIONS: These results indicate that there are trade-offs in terms of signal duration at two levels in pant-hoot production: between call number and duration, and between the relative durations of successive phases. These trade-offs are likely to reflect biomechanical constraints on vocal sequence production. Phase-specific trade-offs also appear to occur between fundamental frequency and call number or duration, potentially reflecting that different phases of the sequence are associated with distinct types of information, linked in different ways to call pitch. Overall, this study highlights the important role of costs and constraints in shaping the temporal and acoustic structure of animal vocal sequences.

Men With a Terminal Illness Relax Their Criteria for Facial Attractiveness.

According to the life history paradigm, in life-threatening conditions, sexual selection criteria are relaxed in order to increase the probability of a last resort reproduction, ultimately contributing to reproductive success. This should be reflected in loosened mating preferences - a process observed in nonhuman animals. Studies investigating this aspect in humans, however, are scarce. This study explored the aesthetic preferences towards facial and nonfacial stimuli in terminally ill patients with heart failure (HF) and their healthy, same-sex peers. The aim was to examine if these two groups of men demonstrate different patterns of aesthetic judgments. Using a 7-point scale, 65 male patients with HF and 143 healthy men evaluated the perceived attractiveness of 15 photographs (five adult male faces, five adult female faces, and five nonfacial pictures). A mixed-design analysis of variance was run to assess group differences in aesthetic preferences. Compared to healthy controls, stimuli. HF patients rated the pictures using significantly higher scores, but this applied only to male and female, but not nonfacial, stimuli. We propose that lower criteria for facial attractiveness in HF patients are linked to relaxation of mate preferences as a result of a life-threatening conditions, and that this process can be an adaptive mating strategy from an ultimate, evolutionary perspective. However, other mechanisms (e.g., seeking social support) may be also responsible for the observed patterns.

Sequential information in a great ape utterance.

Birdsong is a prime example of acoustically sophisticated vocal behaviour, but its complexity has evolved mainly through sexual selection to attract mates and repel sexual rivals. In contrast, non-human primate calls often mediate complex social interactions, but are generally regarded as acoustically simple. Here, we examine arguably the most complex call in great ape vocal communication, the chimpanzee (Pan troglodytes schweinfurthii) 'pant hoot'. This signal consists of four acoustically distinct phases: introduction, build-up, climax and let-down. We applied state-of-the-art Support Vector Machines (SVM) methodology to pant hoots produced by wild male chimpanzees of Budongo Forest, Uganda. We found that caller identity was apparent in all four phases, but most strongly in the low-amplitude introduction and high-amplitude climax phases. Age was mainly correlated with the low-amplitude introduction and build-up phases, dominance rank (i.e. social status) with the high-amplitude climax phase, and context (reflecting activity of the caller) with the low-amplitude let-down phase. We conclude that the complex acoustic structure of chimpanzee pant hoots is linked to a range of socially relevant information in the different phases of the call, reflecting the complex nature of chimpanzee social lives.

The relationship between testosterone and long-distance calling in wild male chimpanzees.

Long-distance calling is a common behaviour in animals that has various important social functions. At a physiological level, calling is often mediated by gonadal hormones such as testosterone (T), particularly when its function is linked to intra-sexual competition for mates or territory. T also plays an important role in the development of vocal characteristics associated with dominance in humans. However, the few available studies of T and vocal behaviour in non-human primates suggest that in primates T has less influence on call production than in other animals. We tested this hypothesis by studying the relationship between T concentrations and pant hooting in wild male chimpanzees (Pan troglodytes schweinfurthii) of the Kanyawara community in the Kibale National Park, Uganda. We found three kinds of correlation. Hourly T averages were positively associated with hourly rates of pant-hooting. Monthly T levels were likewise correlated with monthly rates of pant hooting after controlling for other influences such as fission-fusion rates. Finally, males with high T levels had higher peak frequency at the start of the call climax. These results suggest that T affects the production of pant-hoots in chimpanzees. This implies that the pant-hoot call plays a role in male-male competition. We propose that even in cognitively sophisticated species, endocrine mechanisms can contribute to regulating vocal production.

Chimpanzee lip-smacking facilitates cooperative behaviour.

Signalling plays an important role in facilitating and maintaining affiliative or cooperative interactions in social animals. Social grooming in primates is an example of an interaction that requires coordination between partners but little is known about communicative behaviours facilitating this activity. In this study, we analysed the communication of wild chimpanzees of Budongo Forest, Uganda, as they entered and maintained a naturally occurring cooperative interaction: social grooming. We found that lip-smacking, a distinct multimodal oral gesture produced during grooming, coordinated this activity. Lip-smacking at the beginning of grooming bouts was significantly more often followed by longer and reciprocated bouts than silent grooming initiations. Lip-smacks were more likely to be produced when the risk of termination of the interaction by the recipient was high, for instance when grooming vulnerable body parts. Groomers were also more likely to produce lip-smacks during face-to-face grooming where the visual aspect of the signal could be perceived. Data are consistent with the hypothesis that chimpanzee lip-smacks function to coordinate and prolong social grooming, suggesting that this oral signal is an example of a communicative behaviour facilitating cooperative behaviour in chimpanzees.

The social function of food-associated calls in male chimpanzees.

There is an ongoing debate about the adaptive function of chimpanzee's food-associated calls. Here, we tested a new hypothesis that food-associated calls in male chimpanzees function to signal that the calling individual is likely to initiate or prolong feeding. We propose that the signal functions to coordinate activities between individuals and that its ultimate function is to retain the nearby individuals in proximity. To test this hypothesis, we collected data on social and ecological correlates of food-associates calls in male chimpanzees. The results of this study, which was conducted on the Kanyawara community in the Kibale National Park, Uganda, show that males tended to feed for significantly longer after giving food-associated calls upon initiating feeding than after remaining silent. The type of audience had a significant effect on food calling, with males producing food-associated calls more often when males rather than females and preferred rather than neutral male social partners were in close proximity. However, the total party or male party size did not correlate with food calling behaviors, suggesting that the signal "targets" those in close proximity. Finally, a male feeding partner was more likely to remain with the focal until the end of a feeding bout after the focal gave a food-associated call at the beginning of the feeding bout than when he was silent. These results support our hypothesis and suggest that one of the functions of food calling in chimpanzees might be signaling that the caller is likely to initiate and prolong a feeding bout. This information might be used by receivers to make the decision whether or not to stay with the calling individual on a feeding patch or leave him (fission). The study suggests therefore that ultimately the function of food calling might be to coordinate feeding behaviors between males.

Primate vocal communication: a useful tool for understanding human speech and language evolution?

Language is a uniquely human trait, and questions of how and why it evolved have been intriguing scientists for years. Nonhuman primates (primates) are our closest living relatives, and their behavior can be used to estimate the capacities of our extinct ancestors. As humans and many primate species rely on vocalizations as their primary mode of communication, the vocal behavior of primates has been an obvious target for studies investigating the evolutionary roots of human speech and language. By studying the similarities and differences between human and primate vocalizations, comparative research has the potential to clarify the evolutionary processes that shaped human speech and language. This review examines some of the seminal and recent studies that contribute to our knowledge regarding the link between primate calls and human language and speech. We focus on three main aspects of primate vocal behavior: functional reference, call combinations, and vocal learning. Studies in these areas indicate that despite important differences, primate vocal communication exhibits some key features characterizing human language. They also indicate, however, that some critical aspects of speech, such as vocal plasticity, are not shared with our primate cousins. We conclude that comparative research on primate vocal behavior is a very promising tool for deepening our understanding of the evolution of human speech and language, but much is still to be done as many aspects of monkey and ape vocalizations remain largely unexplored.