Chimpanzee gestural exchanges share temporal structure with human language.

Humans regularly engage in efficient communicative conversations, which serve to socially align individuals1. In conversations, we take fast-paced turns using a human-universal structure of deploying and receiving signals which shows consistent timing across cultures2. We report here that chimpanzees also engage in rapid signal-to-signal turn-taking during face-to-face gestural exchanges with a similar average latency between turns to that of human conversation. This correspondence between human and chimpanzee face-to-face communication points to shared underlying rules in communication. These structures could be derived from shared ancestral mechanisms or convergent strategies that enhance coordinated interactions or manage competition for communicative 'space'.

Many morphs: Parsing gesture signals from the noise.

Parsing signals from noise is a general problem for signallers and recipients, and for researchers studying communicative systems. Substantial efforts have been invested in comparing how other species encode information and meaning, and how signalling is structured. However, research depends on identifying and discriminating signals that represent meaningful units of analysis. Early approaches to defining signal repertoires applied top-down approaches, classifying cases into predefined signal types. Recently, more labour-intensive methods have taken a bottom-up approach describing detailed features of each signal and clustering cases based on patterns of similarity in multi-dimensional feature-space that were previously undetectable. Nevertheless, it remains essential to assess whether the resulting repertoires are composed of relevant units from the perspective of the species using them, and redefining repertoires when additional data become available. In this paper we provide a framework that takes data from the largest set of wild chimpanzee (Pan troglodytes) gestures currently available, splitting gesture types at a fine scale based on modifying features of gesture expression using latent class analysis (a model-based cluster detection algorithm for categorical variables), and then determining whether this splitting process reduces uncertainty about the goal or community of the gesture. Our method allows different features of interest to be incorporated into the splitting process, providing substantial future flexibility across, for example, species, populations, and levels of signal granularity. Doing so, we provide a powerful tool allowing researchers interested in gestural communication to establish repertoires of relevant units for subsequent analyses within and between systems of communication.

Adaptive Party Choice of Low-Ranking Males in Fission-Fusion Dynamics of Chimpanzees in Kalinzu Forest Reserve, Uganda.

Several studies have examined factors that regulate fission-fusion dynamics (FFD) in chimpanzee communities, such as receptive females, predation risks, and food availability. However, the effects of these factors vary between populations. In this study, we conducted focal animal observations of adult males in the M group in Kalinzu to examine the influence of male dominance rank, aggression from other males, the presence of females exhibiting maximum sexual swelling (MS), and fruit abundance on male tendencies of party attendance. We found that low-ranking males spent more time alone than other males when females with MS were absent. In contrast, when females with MS were present, males of all ranks showed a similar tendency of party attendance. We also found that the aggressive interactions increased with the number of males irrespective of the presence or absence of females with MS, and low-ranking males attracted aggression more frequently than higher-ranking males. These results suggest that low-ranking males frequently ranged alone to avoid aggression from other males unless they attended parties to seek mating opportunities. We conclude that low-ranking males have alternative tactics to balance the costs and benefits incurred or gained when attending parties.

Do female bonobos (Pan paniscus) disperse at the onset of puberty? Hormonal and behavioral changes related to their dispersal timing.

Natal dispersal is a milestone in an animal's life history, but its timing in developmental trajectories may differ between species. Although the two Pan species exhibit a similar pattern of female-biased dispersal, female bonobos (P. paniscus) leave their natal groups at an earlier age than female chimpanzees (P. troglodytes). As a preliminary step to explore the dispersal strategies of female bonobos, this study aimed to determine the relations of sexual swelling development, behavioral and hormonal activation, and first ovulation relative to dispersal timing. We measured levels of urinary estrone conjugates (E1C) and pregnanediol glucuronide (PdG) from 14 nulliparous females in wild bonobo groups at Wamba in the Democratic Republic of the Congo, and recorded their copulations with mature males. When close to dispersal, female bonobos exhibited swelling of the sexual skin (labia minora and perianal region) that did not reach the mature stage. Urinary E1C levels and copulation rates increased slightly before dispersal and greatly increased after dispersal. Ovulatory or gestatory signs implied by daily hormone profiles were not detected until one to two years after dispersal. Our findings indicate that female bonobos disperse at an early pubertal stage before ovulatory cycling is established. This earlier dispersal than sexual maturation could allow female bonobos to postpone reproduction-related energy costs until they become familiar with their new group or gain more time finding the group more suitable for successful reproduction in the future before actually settling. Further demographic and genetic data from dispersal to reproduction will help clarify their dispersal strategies.

Physical, behavioral, and hormonal changes in the resumption of sexual receptivity during postpartum infertility in female bonobos at Wamba.

The operational sex ratio (OSR) is used as a predictor for the intensity of mating competition. While many factors affect the OSR, there tends to be a high male bias in primate species with long interbirth intervals and non-seasonal breeding, such as hominid apes. However, the OSR of bonobos (Pan paniscus) is lower than that of chimpanzees (Pan troglodytes), which is thought to reduce competitive and aggressive male behaviors. The low OSR of bonobos is considered to result from the early resumption of female sexual receptivity during postpartum infertility and the receptivity that they continue to show until the late stage of pregnancy. In this study, we aimed to examine the early resumption of sexual receptivity by providing quantitative data on the resumption of maximal swelling (MS) in sexual skin and copulation, and changes in urinary estrone conjugate (E1C) concentrations during postpartum infertility in wild bonobos at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo. An analysis of 9 years of data revealed that females showed the first MS at 225.4 ± 132.7 days after parturition and performed the first copulation at 186.8 ± 137.5 days after parturition, both of which were in the early stage of postpartum infertility. The proportion of days with MS and the frequency of copulation steadily increased subsequently; however, the rate of increase gradually slowed approximately 42-48 months after parturition. There was a significant correlation between the proportion of days with MS and the frequency of copulation in each period for each female. We confirmed that E1C concentrations were significantly higher during the MS phase than during the non-MS phase. Data collected over 15 months on the E1C concentration during MS showed that it increased linearly from the early stage of lactation to the next conception. These results suggest that, although female bonobos do not usually conceive until 49.7 months after parturition, they resume MS and receptivity at a low level of E1C concentration during an early stage of postpartum infertility. This study of female bonobo receptivity and sex hormone changes during the postpartum non-fertile period provides important insights for examining the evolution of low OSR, which has been considered to contribute to peaceful social relationships among bonobos.

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.

The diet and feeding behavior of the black-and-white colobus (Colobus guereza) in the Kalinzu Forest, Uganda.

One of the goals for primate feeding ecology is to understand the factors that affect inter- and intra-specific variations. Therefore, a detailed description of basic feeding ecology in as many populations as possible is necessary and warrants further understanding. The black-and-white colobus (Colobus guereza) or guereza is widely distributed in Africa and is one of the well-studied colobines in terms of their feeding; they demonstrate considerable variation in their diets in response to local conditions. We studied the diet of a group of guerezas in the Kalinzu Forest, Uganda, for over 30 consecutive months using behavioral observation (4308 h in total), phenology, and vegetation surveys. A total of 31 plant species were consumed by the study group. This study group was predominantly folivorous; the majority of their feeding time was involved in feeding on young leaves (87%). However, during certain times of the year, fruits and seeds accounted for 45% of monthly feeding time. Young leaves of Celtis durandii were by far the most important food, which constituted 58% of the total feeding records. There was a significant increase in the consumption of fruits and flowers once young leaf availability was low, but their consumption of fruits did not significantly increase even when fruit availability was high. Their monthly dietary diversity increased as the number of available plants with young leaves declined, suggesting that much of the dietary diversity in the study group may be attributable to the young leaf portion of their diet. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of guerezas in response to local environmental conditions.

Comparisons of between-group differentiation in male kinship between bonobos and chimpanzees.

Patterns of kinship among individuals in different groups have been rarely examined in animals. Two closest living relatives of humans, bonobos and chimpanzees share many characteristics of social systems including male philopatry, whereas one major difference between the two species is the nature of intergroup relationship. Intergroup relationship is basically antagonistic and males sometimes kill individuals of other groups in chimpanzees, whereas it is much more moderate in bonobos and copulations between individuals of different groups are often observed during intergroup encounters. Such behavioural differences may facilitate more frequent between-group male gene flow and greater between-group differentiation in male kinship in bonobos than in chimpanzees. Here we compared differences between average relatedness among males within groups and that among males of neighbouring groups, and between-group male genetic distance between bonobos and chimpanzees. Contrary to expectation, the differences between average relatedness among males within groups and that among males of neighbouring groups were significantly greater in bonobos than in chimpanzees. There were no significant differences in autosomal and Y-chromosomal between-group male genetic distance between the two species. Our results showed that intergroup male kinship is similarly or more differentiated in bonobos than in chimpanzees.

No impact of strongylid infections on the detection of Plasmodium spp. in faeces of western lowland gorillas and eastern chimpanzees.

BACKGROUND: Although a high genetic diversity of Plasmodium spp. circulating in great apes has been revealed recently due to non-invasive methods enabling detection in faecal samples, little is known about the actual mechanisms underlying the presence of Plasmodium DNA in faeces. Great apes are commonly infected by strongylid nematodes, including hookworms, which cause intestinal bleeding. The impact of strongylid infections on the detection of Plasmodium DNA in faeces was assessed in wild, western, lowland gorillas from Dzanga Sangha Protected Areas, Central African Republic and eastern chimpanzees from Kalinzu Forest Reserve, Uganda. METHODS: Fifty-one faecal samples from 22 habituated gorillas and 74 samples from 15 habituated chimpanzees were analysed using Cytochrome-b PCR assay and coprological methods. RESULTS: Overall, 26.4% of the analysed samples were positive for both Plasmodium spp. and strongylids. However, the results showed no significant impact of intensity of infections of strongylids on detection of Plasmodium DNA in gorilla and chimpanzee faeces. CONCLUSION: Bleeding caused by strongylid nematode Necator spp. cannot explain the presence of Plasmodium DNA in ape faeces.

Development of anti-HIV peptides based on a viral capsid protein.

Peptide inhibitors with cell permeability targeting an HIV-1 capsid (CA) protein might make therapeutic by regulating HIV-1 replication. Overlapping fragment peptide libraries covering the whole sequence of an HIV-1 CA protein have been synthesized with the addition of an octa-arginyl moiety to increase their cell permeability. Amongst these peptides, several compounds which inhibit the HIV-1 replication cycle have been found. Conjugation of cell-penetrating functions such as an octa-arginyl group to individual peptides in combination with the addition of chloroquine in cell-based anti-HIV assays was previously proven to be a useful assay method with which to search for active peptides. Anti-HIV assays have been performed in the presence or absence of chloroquine and found that most of compounds have higher anti-HIV activity in the presence, rather than in the absence of chloroquine. Some potent seeds as anti-HIV agents might naturally lie hidden in CA proteins, and could become useful leads to HIV inhibitors.

A comparative molecular survey of malaria prevalence among Eastern chimpanzee populations in Issa Valley (Tanzania) and Kalinzu (Uganda).

BACKGROUND: Habitat types can affect vector and pathogen distribution and transmission dynamics. The prevalence and genetic diversity of Plasmodium spp. in two eastern chimpanzee populations-Kalinzu Forest Reserve, Uganda and Issa Valley, Tanzania-inhabiting different habitat types was investigated. As a follow up study the effect of host sex and age on infections patterns in Kalinzu Forest Reserve chimpanzees was determined. METHODS: Molecular methods were employed to detect Plasmodium DNA from faecal samples collected from savanna-woodland (Issa Valley) and forest (Kalinzu Forest Reserve) chimpanzee populations. RESULTS: Based on a Cytochrome-b PCR assay, 32 out of 160 Kalinzu chimpanzee faecal samples were positive for Plasmodium DNA, whilst no positive sample was detected in 171 Issa Valley chimpanzee faecal samples. Sequence analysis revealed that previously known Laverania species (Plasmodium reichenowi, Plasmodium billbrayi and Plasmodium billcollinsi) are circulating in the Kalinzu chimpanzees. A significantly higher proportion of young individuals were tested positive for infections, and switching of Plasmodium spp. was reported in one individual. Amongst the positive individuals sampled more than once, the success of amplification of Plasmodium DNA from faeces varied over sampling time. CONCLUSION: The study showed marked differences in the prevalence of malaria parasites among free ranging chimpanzee populations living in different habitats. In addition, a clear pattern of Plasmodium infections with respect to host age was found. The results presented in this study contribute to understanding the ecological aspects underlying the malaria infections in the wild. Nevertheless, integrative long-term studies on vector abundance, Plasmodium diversity during different seasons between sites would provide more insight on the occurrence, distribution and ecology of these pathogens.

Sex Differences in Object Manipulation in Wild Immature Chimpanzees (Pan troglodytes schweinfurthii) and Bonobos (Pan paniscus): Preparation for Tool Use?

Sex differences in immatures predict behavioural differences in adulthood in many mammal species. Because most studies have focused on sex differences in social interactions, little is known about possible sex differences in 'preparation' for adult life with regards to tool use skills. We investigated sex and age differences in object manipulation in immature apes. Chimpanzees use a variety of tools across numerous contexts, whereas bonobos use few tools and none in foraging. In both species, a female bias in adult tool use has been reported. We studied object manipulation in immature chimpanzees at Kalinzu (Uganda) and bonobos at Wamba (Democratic Republic of Congo). We tested predictions of the 'preparation for tool use' hypothesis. We confirmed that chimpanzees showed higher rates and more diverse types of object manipulation than bonobos. Against expectation, male chimpanzees showed higher object manipulation rates than females, whereas in bonobos no sex difference was found. However, object manipulation by male chimpanzees was play-dominated, whereas manipulation types of female chimpanzees were more diverse (e.g., bite, break, carry). Manipulation by young immatures of both species was similarly dominated by play, but only in chimpanzees did it become more diverse with age. Moreover, in chimpanzees, object types became more tool-like (i.e., sticks) with age, further suggesting preparation for tool use in adulthood. The male bias in object manipulation in immature chimpanzees, along with the late onset of tool-like object manipulation, indicates that not all (early) object manipulation (i.e., object play) in immatures prepares for subsistence tool use. Instead, given the similarity with gender differences in human children, object play may also function in motor skill practice for male-specific behaviours (e.g., dominance displays). In conclusion, even though immature behaviours almost certainly reflect preparation for adult roles, more detailed future work is needed to disentangle possible functions of object manipulation during development.

First records of tool-set use for ant-dipping by Eastern chimpanzees (Pan troglodytes schweinfurthii) in the Kalinzu Forest Reserve, Uganda.

Chimpanzees at numerous study sites are known to prey on army ants by using a single wand to dip into the ant nest or column. However, in Goualougo (Republic of Congo) in Central Africa, chimpanzees use a different technique, use of a woody sapling to perforate the ant nest, then use of a herb stem as dipping tool to harvest the army ants. Use of a tool set has also been found in Guinea, West Africa: at Seringbara in the Nimba Mountains and at nearby Bossou. There are, however, no reports for chimpanzees in East Africa. We observed use of such a tool set in Kalinzu, Uganda, for the first time by Eastern chimpanzees. This behavior was observed among one group of chimpanzees at Kalinzu (S-group) but not among the adjacent group (M-group) with partly overlapping ranging areas despite the fact that the latter group has been under intensive observation since 1997. In Uganda, ant-dipping has not been observed in the northern three sites (Budongo, Semliki, and Kibale) but has been observed or seems to occur in the southern sites (Kalinzu and Bwindi), which suggests that ant-dipping was invented by and spread from the southern region after the northern and southern forest blocks became separated. Use of a tool-set by only one group at Kalinzu further suggests that this behavior was recently invented and has not yet spread to the other group via migrating females.

Turning Peptide Ligands into Small-Molecule Inhibitors of Protein-Protein Interactions.

Proline makeover: Truncation and extensive chemical modification of a peptide ligand yielded a biologically active, cell-permeable, peptidomimetic, small-molecule inhibitor of a protein-protein interaction. A key step in this transformation was the replacement of a tetraproline motif by two conformationally constrained diproline units that retain the molecule's PPII helix.

Cultural differences in ant-dipping tool length between neighbouring chimpanzee communities at Kalinzu, Uganda.

Cultural variation has been identified in a growing number of animal species ranging from primates to cetaceans. The principal method used to establish the presence of culture in wild populations is the method of exclusion. This method is problematic, since it cannot rule out the influence of genetics and ecology in geographically distant populations. A new approach to the study of culture compares neighbouring groups belonging to the same population. We applied this new approach by comparing ant-dipping tool length between two neighbouring communities of chimpanzees (Pan troglodytes schweinfurthii) in the Kalinzu Forest, Uganda. Ant-dipping tool length varies across chimpanzee study sites in relation to army ant species (Dorylus spp.) and dipping location (nest vs. trail). We compared the availability of army ant species and dipping tool length between the two communities. M-group tools were significantly longer than S-group tools, despite identical army ant target species availabilities. Moreover, tool length in S-group was shorter than at all other sites where chimpanzees prey on epigaeic ants at nests. Considering the lack of ecological differences between the two communities, the tool length difference appears to be cultural. Our findings highlight how cultural knowledge can generate small-scale cultural diversification in neighbouring chimpanzee communities.

Molecular phylogeny of anoplocephalid tapeworms (Cestoda: Anoplocephalidae) infecting humans and non-human primates.

Anoplocephalid tapeworms of the genus Bertiella Stiles and Hassall, 1902 and Anoplocephala Blanchard, 1848, found in the Asian, African and American non-human primates are presumed to sporadic ape-to-man transmissions. Variable nuclear (5.8S-ITS2; 28S rRNA) and mitochondrial genes (cox1; nad1) of isolates of anoplocephalids originating from different primates (Callicebus oenanthe, Gorilla beringei, Gorilla gorilla, Pan troglodytes and Pongo abelii) and humans from various regions (South America, Africa, South-East Asia) were sequenced. In most analyses, Bertiella formed a monophyletic group within the subfamily Anoplocephalinae, however, the 28S rRNA sequence-based analysis indicated paraphyletic relationship between Bertiella from primates and Australian marsupials and rodents, which should thus be regarded as different taxa. Moreover, isolate determined as Anoplocephala cf. gorillae from mountain gorilla clustered within the Bertiella clade from primates. This either indicates that A. gorillae deserves to be included into the genus Bertiella, or, that an unknown Bertiella species infects also mountain gorillas. The analyses allowed the genetic differentiation of the isolates, albeit with no obvious geographical or host-related patterns. The unexpected genetic diversity of the isolates studied suggests the existence of several Bertiella species in primates and human and calls for revision of the whole group, based both on molecular and morphological data.

Anti-HIV screening for cell-penetrating peptides using chloroquine and identification of anti-HIV peptides derived from matrix proteins.

Previously, compounds which inhibit the HIV-1 replication cycle were found in overlapping peptide libraries covering the whole sequence of an HIV-1 matrix (MA) protein constructed with the addition of an octa-arginyl group. The two top lead compounds are sequential fragments MA-8L and MA-9L. In the present study, the addition of chloroquine in cell-based anti-HIV assays was proven to be an efficient method with which to find anti-HIV compounds among several peptides conjugated by cell-penetrating signals such as an octa-arginyl group: the conjugation of an octa-arginyl group to individual peptides contained in whole proteins in combination with the addition of chloroquine in cells is a useful assay method to search active peptides. To find more potent fragment peptides, individual peptides between MA-8L and MA-9L, having the same peptide chain length but with sequences shifted by one amino acid residue, were synthesized in this paper and their anti-HIV activity was evaluated with an anti-HIV assay using chloroquine. As a result, the peptides in the C-terminal side of the series, which are relatively close to MA-9L, showed more potent inhibitory activity against both X4-HIV-1 and R5-HIV-1 than the peptides in the N-terminal side.

Chimpanzees and bonobos differ in intrinsic motivation for tool use.

Tool use in nonhuman apes can help identify the conditions that drove the extraordinary expansion of hominin technology. Chimpanzees and bonobos are our closest living relatives. Whereas chimpanzees are renowned for their tool use, bonobos use few tools and none in foraging. We investigated whether extrinsic (ecological and social opportunities) or intrinsic (predispositions) differences explain this contrast by comparing chimpanzees at Kalinzu (Uganda) and bonobos at Wamba (DRC). We assessed ecological opportunities based on availability of resources requiring tool use. We examined potential opportunities for social learning in immature apes. Lastly, we investigated predispositions by measuring object manipulation and object play. Extrinsic opportunities did not explain the tool use difference, whereas intrinsic predispositions did. Chimpanzees manipulated and played more with objects than bonobos, despite similar levels of solitary and social play. Selection for increased intrinsic motivation to manipulate objects likely also played an important role in the evolution of hominin tool use.

Synthetic Peptides as Protein Mimics.

The design and generation of molecules capable of mimicking the binding and/or functional sites of proteins represents a promising strategy for the exploration and modulation of protein function through controlled interference with the underlying molecular interactions. Synthetic peptides have proven an excellent type of molecule for the mimicry of protein sites because such peptides can be generated as exact copies of protein fragments, as well as in diverse chemical modifications, which includes the incorporation of a large range of non-proteinogenic amino acids as well as the modification of the peptide backbone. Apart from extending the chemical and structural diversity presented by peptides, such modifications also increase the proteolytic stability of the molecules, enhancing their utility for biological applications. This article reviews recent advances by this and other laboratories in the use of synthetic protein mimics to modulate protein function, as well as to provide building blocks for synthetic biology.