Death among geladas (Theropithecus gelada): a broader perspective on mummified infants and primate thanatology

Despite intensive study in humans, responses to dying and death have been a neglected area of research in other social mammals, including nonhuman primates. Two recent reports [Anderson JR, Gillies A, Lock LC. 2010. Pan thanatology. Current Biology 20:R349–R351; Biro D, Humle T, Koops K, Souse C, Hayashi M, Matsuzawa T. 2010. Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Current Biology 20:R351–R352] offered exciting new insights into behavior toward dying and dead conspecifics in our closest living relatives—chimpanzees. Here, we provide a comparative perspective on primate thanatology using observations from a more distant human relative—gelada monkeys (Theropithecus gelada)—and discuss how gelada reactions to dead and dying groupmates differ from those recently reported for chimpanzees. Over a 3.75‐year study period, we observed 14 female geladas at Guassa, Ethiopia carrying dead infants from 1 hr to ≥48 days after death. Dead infants were carried by their mothers, other females in their group, and even by females belonging to other groups. Like other primate populations in which extended (>10 days) infant carrying after death has been reported, geladas at Guassa experience an extreme climate for primates, creating conditions which may favor slower rates of decomposition of dead individuals. We also witnessed the events leading up to the deaths of two individuals and the responses by groupmates to these dying individuals. Our results suggest that while chimpanzee mothers are not unique among primates in carrying their dead infants for long periods, seemingly “compassionate” caretaking behavior toward dying groupmates may be unique to chimpanzees among nonhuman primates (though it remains unknown whether such “compassionate” behavior occurs outside captivity). Am. J. Primatol. 73:405–409, 2011. © 2010 Wiley‐Liss, Inc.     

Male yawning is more contagious than female yawning among chimpanzees (Pan troglodytes)

Yawn contagion is not restricted to humans and has also been reported for several non-human animal species, including chimpanzees (Pan troglodytes). Contagious yawning may lead to synchronisation of behaviour. However, the function of contagious yawning is relatively understudied. In this study, we investigated the function of contagious yawning by focusing on two types of signal providers: close social associates and leaders. We provided a captive chimpanzee colony with videos of all individuals of their own group that were either yawning, or at rest. Consistent with other studies, we demonstrated that yawning is contagious for chimpanzees, yet we did not find any effect of relationship quality on yawn contagion. However, we show that yawn contagion is significantly higher when the video model is a yawning male than when the video model was a yawning female, and that this effect is most apparent among males. As males are dominant in chimpanzee societies, male signals may be more relevant to the rest of the group than female signals. Moreover, since chimpanzees form male-bonded societies, male signals are especially relevant for other males. Therefore, we suggest that the sex-differences of yawning contagion among chimpanzees reflect the function of yawning in the synchronisation of behaviour.     

Evolutionary precursors of social norms in chimpanzees: a new approach

Moral behaviour, based on social norms, is commonly regarded as a hallmark of humans. Hitherto, humans are perceived to be the only species possessing social norms and to engage in moral behaviour. There is anecdotal evidence suggesting their presence in chimpanzees, but systematic studies are lacking. Here, we examine the evolution of human social norms and their underlying psychological mechanisms. For this, we distinguish between conventions, cultural social norms and universal social norms. We aim at exploring whether chimpanzees possess evolutionary precursors of universal social norms seen in humans. Chimpanzees exhibit important preconditions for their presence and enforcement: tolerant societies, well-developed social-cognitive skills and empathetic competence. Here, we develop a theoretical framework for recognizing different functional levels of social norms and distinguish them from mere statistical behavioural regularities. Quasi social norms are found where animals behave functionally moral without having moral emotions. In proto social norms, moral emotions might be present but cannot be collectivized due to the absence of a uniquely human psychological trait, i.e. shared intentionality. Human social norms, whether they are universal or cultural, involve moral emotions and are collectivized. We will discuss behaviours in chimpanzees that represent potential evolutionary precursors of human universal social norms, with special focus on social interactions involving infants. We argue that chimpanzee infants occupy a special status within their communities and propose that tolerance towards them might represent a proto social norm. Finally, we discuss possible ways to test this theoretical framework.     

Inbreeding Avoidance in Male Primates: A Response to Female Mate Choice?

Inbreeding often has negative fitness consequences for primates, which have led to the evolution of inbreeding avoidance strategies in a number of species. In polygynous primates, females may suffer a higher fitness cost from inbreeding than males and are thus expected to exhibit a lower tolerance for inbreeding. Nevertheless, it is apparent that inbreeding avoidance behaviours are common in both female and male polygynous primates. In this perspectives article, I review the evidence that female mate choice can lead to male inbreeding avoidance behaviours in polygynous primates. I conclude that male inbreeding avoidance may be strongly driven by female mate choice at both proximate and ultimate levels. To better understand the extent to which this pattern applies across the primate order, studies are needed on the separate effects of participating in inbred matings and producing inbred offspring on male and female lifetime reproductive success . It would also be useful to examine how inbreeding avoidance strategies vary across primate mating systems. Finally, measuring the covariance between female choice and male inbreeding avoidance behaviour, and between male inbreeding avoidance behaviour and male fitness, would help to clarify the role of female mate choice in the evolution of male inbreeding avoidance.     

Pan thanatology

Chimpanzees' immediate responses to the death of a group-member have rarely been described. Exceptions include maternal care towards dead infants, and frenzied excitement and alarm following the sudden, traumatic deaths of older individuals [1-5]. Some wild chimpanzees die in their night nest [6], but the immediate effect this has on others is totally unknown. Here, with supporting video material, we describe the peaceful demise of an elderly female in the midst of her group. Group responses include pre-death care of the female, close inspection and testing for signs of life at the moment of death, male aggression towards the corpse, all-night attendance by the deceased's adult daughter, cleaning the corpse, and later avoidance of the place where death occurred. Without death-related symbols or rituals, chimpanzees show several behaviours that recall human responses to the death of a close relative.     

Male care and exploitation of infants in Papio anubis

Male olive baboons decreased the probability of their being threatened by other males, and increased their relative dominance, if they were carrying infants during encounters with other males. Carrying of infants by males could be hazardous to the infants. However, males also showed other behaviours which were beneficial to infants. Choice of infant for ‘exploting’ and certain forms of ‘caretaking’ by males varied with the age of the infant. Both exploitation and caretaking by males were almost completely restricted to those infants which were born after the males' immigration into the infants' troop. Males which exploited infants most often also showed most caretaking behaviours and had resided in that troop the longest. Males that had infants carried against them by other males most often were the most dominant and the youngest sexually mature males. Males still residing in their natal troop chose their matrilineal siblings most often for exploiting and certain caretaking behaviours. The overall effects of close male-infant relations on the fitness of the male and the infant are discussed.     

Percussive technology in human evolution: an introduction to a comparative approach in fossil and living primates

Percussive technology is part of the behavioural suite of several fossil and living primates. Stone Age ancestors used lithic artefacts in pounding activities, which could have been most important in the earliest stages of stone working. This has relevant evolutionary implications, as other primates such as chimpanzees and some monkeys use stone hammer-and-anvil combinations to crack hard-shelled foodstuffs. Parallels between primate percussive technologies and early archaeological sites need to be further explored in order to assess the emergence of technological behaviour in our evolutionary line, and firmly establish bridges between Primatology and Archaeology. What are the anatomical, cognitive and ecological constraints of percussive technology? How common are percussive activities in the Stone Age and among living primates? What is their functional significance? How similar are archaeological percussive tools and those made by non-human primates? This issue of Phil. Trans. addresses some of these questions by presenting case studies with a wide chronological, geographical and disciplinary coverage. The studies presented here cover studies of Brazilian capuchins, captive chimpanzees and chimpanzees in the wild, research on the use of percussive technology among modern humans and recent hunter–gatherers in Australia, the Near East and Europe, and archaeological examples of this behaviour from a million years ago to the Holocene. In summary, the breadth and depth of research compiled here should make this issue of Philosophical Transactions of the Royal Society B, a landmark step forward towards a better understanding of percussive technology, a unique behaviour shared by some modern and fossil primates.     

Male sexual harassment alters female social behaviour towards other females

Male harassment of females to gain mating opportunities is a consequence of an evolutionary conflict of interest between the sexes over reproduction and is common among sexually reproducing species. Male Trinidadian guppies Poecilia reticulata spend a large proportion of their time harassing females for copulations and their presence in female social groups has been shown to disrupt female-female social networks and the propensity for females to develop social recognition based on familiarity. In this study, we investigate the behavioural mechanisms that may lead to this disruption of female sociality. Using two experiments, we test the hypothesis that male presence will directly affect social behaviours expressed by females towards other females in the population. In experiment one, we tested for an effect of male presence on female shoaling behaviour and found that, in the presence of a free-swimming male guppy, females spent shorter amounts of time with other females than when in the presence of a free-swimming female guppy. In experiment two, we tested for an effect of male presence on the incidence of aggressive behaviour among female guppies. When males were present in a shoal, females exhibited increased levels of overall aggression towards other females compared with female only shoals. Our work provides direct evidence that the presence of sexually harassing males alters female-female social behaviour, an effect that we expect will be recurrent across taxonomic groups.     

Morphometric variables related to metabolic profile in captive chimpanzees (Pan troglodytes)

Obesity is a risk factor for several diseases including type 2 diabetes and cardiovascular disease. The aim of this study was to compare the relationships of waist circumference and body weight with circulating markers of metabolic, cardiovascular, and hepatic function in chimpanzees (Pan troglodytes). After a 12-h fast, blood was collected from 39 adult captive chimpanzees for measurement of serum glucose, BUN, creatinine, albumin, cholesterol, ALT, AST, ALP, total and direct bilirubin, triglyceride, and insulin, and waist circumference and body weight were measured. Waist circumference was positively correlated with systolic and diastolic blood pressure, glucose, insulin resistance as estimated by the homeostatic model assessment method, and albumin in female chimpanzees and with triglyceride in female and male chimpanzees. Body weight was correlated significantly with systolic and diastolic blood pressure in female chimpanzees and triglyceride in male chimpanzees. Male chimpanzees were heavier and had lower diastolic blood pressure, greater creatinine, albumin, AST, ALP, total bilirubin, and direct bilirubin values than did female chimpanzees. The relationships between waist circumference and blood pressure and triglyceride are consistent with those reported in humans and other primate species. In conclusion, our study is the first work to demonstrate a relationship between waist circumference and metabolic risk factors in chimpanzees. Results demonstrated that waist circumference was associated with more metabolic risk factors than was body weight, particularly in female chimpanzees.     

Sex‐biased dispersal of human ancestors

Some anthropologists and primatologists have argued that, judging by extant chimpanzees and humans, which are female‐biased dispersers, the common ancestors of humans and chimpanzees were also female‐biased dispersers. It has been thought that sex‐biased dispersal patterns have been genetically transmitted for millions of years. However, this character has changed many times with changes in environment and life‐form during human evolution and historical times. I examined life‐form and social organization of nonhuman primates, among them gatherers (foragers), hunter‐gatherers, agriculturalists, industrialists, and modern and extant humans. I conclude that dispersal patterns changed in response to environmental conditions during primate and human evolution.     

Nepotistic cooperation in non-human primate groups

Darwin was struck by the many similarities between humans and other primates and believed that these similarities were the product of common ancestry. He would be even more impressed by the similarities if he had known what we have learned about primates over the last 50 years. Genetic kinship has emerged as the primary organizing force in the evolution of primate social organization and the patterning of social behaviour in non-human primate groups. There are pronounced nepotistic biases across the primate order, from tiny grey mouse lemurs (Microcebus murinus) that forage alone at night but cluster with relatives to sleep during the day, to cooperatively breeding marmosets that rely on closely related helpers to rear their young, rhesus macaque (Macaca mulatta) females who acquire their mother''s rank and form strict matrilineal dominance hierarchies, male howler monkeys that help their sons maintain access to groups of females and male chimpanzees (Pan troglodytes) that form lasting relationships with their brothers. As more evidence of nepotism has accumulated, important questions about the evolutionary processes underlying these kin biases have been raised. Although kin selection predicts that altruism will be biased in favour of relatives, it is difficult to assess whether primates actually conform to predictions derived from Hamilton''s rule: br > c. In addition, other mechanisms, including contingent reciprocity and mutualism, could contribute to the nepotistic biases observed in non-human primate groups. There are good reasons to suspect that these processes may complement the effects of kin selection and amplify the extent of nepotistic biases in behaviour.     

Perspectives on object manipulation and action grammar for percussive actions in primates

The skill of object manipulation is a common feature of primates including humans, although there are species-typical patterns of manipulation. Object manipulation can be used as a comparative scale of cognitive development, focusing on its complexity. Nut cracking in chimpanzees has the highest hierarchical complexity of tool use reported in non-human primates. An analysis of the patterns of object manipulation in naive chimpanzees after nut-cracking demonstrations revealed the cause of difficulties in learning nut-cracking behaviour. Various types of behaviours exhibited within a nut-cracking context can be examined in terms of the application of problem-solving strategies, focusing on their basis in causal understanding or insightful intentionality. Captive chimpanzees also exhibit complex forms of combinatory manipulation, which is the precursor of tool use. A new notation system of object manipulation was invented to assess grammatical rules in manipulative actions. The notation system of action grammar enabled direct comparisons to be made between primates including humans in a variety of object-manipulation tasks, including percussive-tool use.     

Repeatability of Host Female and Male Aggression Towards a Brood Parasite

Current research on behavioural consistency showed that various types of animal behaviour are highly repeatable in the context of mate choice, exploration and parental care, including nest protection. However, the repeatability of aggressive nest defence has not yet been studied in hosts of brood parasites, although host aggression against adult parasites represents a crucial line of antiparasitic defences. Here, we investigated the between‐season repeatability of the great reed warbler (Acrocephalus arundinaceus) aggression towards a stuffed dummy of the brood parasitic common cuckoo (Cuculus canorus). We found that under the relatively stable risk of brood parasitism across breeding seasons, female responses to the cuckoo were highly repeatable, whereas male responses were variable. We suggest that the potential explanation for the observed patterns of female and male behaviours may lie in female's prominent roles in offspring care and nest protection, and in her lower renesting potential in comparison with that of males. However, further studies on the relationship between host aggression and other types of behaviours (host personality) and their fitness consequences under the fluctuating parasitism pressures are required to clarify the adaptive significance of aggressive behaviour observed in hosts of brood parasites.     

Explaining human uniqueness: genome interactions with environment, behaviour and culture

What makes us human? Specialists in each discipline respond through the lens of their own expertise. In fact, 'anthropogeny' (explaining the origin of humans) requires a transdisciplinary approach that eschews such barriers. Here we take a genomic and genetic perspective towards molecular variation, explore systems analysis of gene expression and discuss an organ-systems approach. Rejecting any 'genes versus environment' dichotomy, we then consider genome interactions with environment, behaviour and culture, finally speculating that aspects of human uniqueness arose because of a primate evolutionary trend towards increasing and irreversible dependence on learned behaviours and culture - perhaps relaxing allowable thresholds for large-scale genomic diversity.     

Social learning and teaching in chimpanzees

There is increasing evidence that some behavioural differences between groups of chimpanzees can be attributed neither to genetic nor to ecological variation. Such differences are likely to be maintained by social learning. While humans teach their offspring, and acquire cultural traits through imitative learning, there is little evidence of such behaviours in chimpanzees. However, by appealing only to incremental changes in motivation, attention and attention-soliciting behaviour, and without expensive changes in cognition, we can hypothesise the possible emergence of imitation and pedagogy in evolutionary history.     

Hierarchy and social status in Budongo chimpanzees

The status hierarchy is fundamental in the lives of male chimpanzees. This study describes the dominance interactions and social status among adult male chimpanzees of the Sonso community in the Budongo Forest Reserve, Uganda, during the period that they were first studied (1994 and 1995). Social dominance is typically measured using the behaviour of either the subordinate or the dominant individual, but a relationship is dependent on the behaviour of both parties and this study explicitly used both subordinate and dominant behaviours to investigate the status hierarchy. Among adult males of the Sonso community, agonistic interactions occurred at a low rate and pant-grunts were rare, but males could be ranked into separate hierarchies of agonistic dominance and pant-grunting (labelled respect) using ratios of behaviour performed/behaviour received. These hierarchies were combined to form a single hierarchy of social status that divided the males among five distinct status levels. The highest status level was held by an alliance between two males who replaced the previous alpha male during the first part of the study. Neither male in this alliance partnership pant-grunted to the other, although the reason for cooperative behaviour was unclear. Although the nominally beta male was treated as such by other adult males, he achieved surprisingly little mating success. Budongo Forest chimpanzees do not warrant the sometimes-expressed view that they are non-aggressive and peaceable and the broad pattern of their status interactions matches with that seen in other chimpanzee populations.     

How chimpanzees look at pictures: a comparative eye-tracking study

Surprisingly little is known about the eye movements of chimpanzees, despite the potential contribution of such knowledge to comparative cognition studies. Here, we present the first examination of eye tracking in chimpanzees. We recorded the eye movements of chimpanzees as they viewed naturalistic pictures containing a full-body image of a chimpanzee, a human or another mammal; results were compared with those from humans. We found a striking similarity in viewing patterns between the two species. Both chimpanzees and humans looked at the animal figures for longer than at the background and at the face region for longer than at other parts of the body. The face region was detected at first sight by both species when they were shown pictures of chimpanzees and of humans. However, the eye movements of chimpanzees also exhibited distinct differences from those of humans; the former shifted the fixation location more quickly and more broadly than the latter. In addition, the average duration of fixation on the face region was shorter in chimpanzees than in humans. Overall, our results clearly demonstrate the eye-movement strategies common to the two primate species and also suggest several notable differences manifested during the observation of pictures of scenes and body forms.     

Sexual Size Dimorphism,Canine Dimorphism,and Male-Male Competition in Primates

Sexual size dimorphism is generally associated with sexual selection via agonistic male competition in nonhuman primates. These primate models play an important role in understanding the origins and evolution of human behavior. Human size dimorphism is often hypothesized to be associated with high rates of male violence and polygyny. This raises the question of whether human dimorphism and patterns of male violence are inherited from a common ancestor with chimpanzees or are uniquely derived. Here I review patterns of, and causal models for, dimorphism in humans and other primates. While dimorphism in primates is associated with agonistic male mate competition, a variety of factors can affect male and female size, and thereby dimorphism. The causes of human sexual size dimorphism are uncertain, and could involve several non-mutually-exclusive mechanisms, such as mate competition, resource competition, intergroup violence, and female choice. A phylogenetic reconstruction of the evolution of dimorphism, including fossil hominins, indicates that the modern human condition is derived. This suggests that at least some behavioral similarities with Pan associated with dimorphism may have arisen independently, and not directly from a common ancestor.     

Birth and perinatal behaviour in family groups of the common marmoset (Callithrix jacchus jacchus), compared to other primates

Birth and perinatal behaviour in five family groups of the common marmoset are described. Information is given on 16 births, seven of which are described in detail.The birth process was divided into five stages; data are presented on the durations of the stages and the behaviours exhibited by the female in each stage.Infant marmosets cling unaided to the pelage of the female from birth, and the behaviour of neonates and the reactions of the female to infants are discussed.The interactions of other group members to the mother and neonates were analysed. The adult male's first interactions with the neonates appeared to occur much earlier (less than one hour after birth) than in other non-human primate species.Perinatal behaviour in marmosets is compared to that recorded in other non-human primate species and discussed in relation to the social organisation of C. j. jacchus.     

The role of female dominance hierarchies in the mating behaviour of mosquitofish

While studies of sexual selection focus primarily on female choice and male-male competition, males should also exert mate choice in order to maximize their reproductive success. We examined male mate choice in mosquitofish, Gambusia holbrooki, with respect to female size and female dominance. We found that the number of mating attempts made by a male was predicted by the dominance rank of females in a group, with dominant females attracting more mating attempts than subordinates. The number of mating attempts made by males was independent of the female size. The observed bias in the number of mating attempts towards dominant females may be driven either by straightforward male mate choice, since dominance and female fecundity are often closely related, or via the dominant females mediating male mating behaviour by restricting their access to subordinate females.