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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.

Human visitors affect the behavior of captive animals, which is the so-called visitor effect. The number and behavior of visitors may influence stress-related behaviors in captive animals, such as self-scratching, yawning, and visitor-directed vigilance. A captive social group setting that resembles the setting in the wild can be applied to alleviate such negative visitor effects and facilitate social behavior and interactions between individuals. In this study, we examined how the number and behavior of visitors are related to stress-related behaviors of a captive mixed-species gibbon pair comprising a yellow-cheek gibbon (Nomascus gabriellae) and a white-handed gibbon (Hylobates lar). The two gibbons were put through a process of separation during the study period, and we examined whether the social isolation stimulated the visitor effect. The frequencies of stress-related behaviors of the gibbons increased and social playing between them decreased with increasing visitors, particularly after social isolation. In the indoor enclosure, the gibbons increased their visitor-directed vigilance when visitors shouted or struck the glass partition. Our findings indicate that the number and behavior of visitors negatively affect captive gibbons and that a mixed-species social setting can help gibbons reduce visitor-induced stress.

Mothers are the most fundamental individuals for the survival and development of their immature offspring. Sex-biased dispersal has an effect on strong and long-lasting social bonding between mothers and their philopatric offspring. Nepotistic relationships are often seen in species with male-biased dispersal but less frequently in species with female-biased dispersal. Bonobos are unique among female-biased dispersal primates in that the females are codominant with males, exert influence on the mating opportunities of their mature sons, and tolerate each other regardless of relatedness. Few studies on bonobos have examined sex differences in social relationships between juveniles and their mothers, and how this relates to mother–son and female–female cooperative relationships amongst adults. We investigated whether the association index of juveniles with their mothers changed with age depending on the sex of the juveniles in parties of bonobos at Wamba, the Democratic Republic of the Congo. We found that female bonobos had decreased party associations with their mothers prior to their emigration from the natal group, while male bonobos maintained relatively high party associations with their mothers. These results indicate that sex differences that emerge during the juvenile period in bonobos in their spatial relationships with their mothers differ from previous findings on chimpanzees, spider monkeys, and muriquis, in which philopatric sons tend to spend less time in proximity to their mothers and disperse earlier than, or at a similar age to, daughters. The contrasts between bonobos and other primate species suggest that the high social status of female bonobos relative to that of males may facilitate the extension of maternal support for their philopatric sons, and that high tolerance among unrelated females may enable the spatial independence of daughters from their mothers at an earlier stage.

Infectious diseases constitute one of the major threats to African great apes. Bonobos (Pan paniscus) may be particularly vulnerable to the transmission of infectious diseases because of their cohesive grouping and frequent social and sexual interactions between groups. Here we report two cases of a flu-like illness and possible transmission of the illness among neighboring wild bonobo groups at Wamba, DR Congo. The first flu-like outbreak started in the PE group on July 28, 2013, 2 days after they had encounters with the BI and PW groups. All PE members, except for one infant, subsequently developed flu-like symptoms, including coughing and running nose. The second flu-like outbreak occurred in the E1 group on October 14, 2013, after E1 had encountered the PE group and the two groups stayed together from October 7 to 11. Eleven out of the 15 observed party members developed symptoms over the next 4 days. The pathogens underlying the two outbreaks may have been related as two temporary immigrant females, who had previously shown symptoms while in the PE group, stayed briefly in the E1 group during the second outbreak, but did not show any symptoms.

Female bonobos exhibit prolonged receptivity, one suggested function of which is to lower male mating competition. However, it is questionable whether easier access to receptive females can reduce male-male competition, given the exclusive nature of male reproductive success. We tested whether males could determine the fertile phase of females. We found that ovulation probability predicted male mating effort. High-ranking males copulated with females with higher fertility, and male-male agonistic interactions increased when there were fertile females in the party. When there were multiple females with maximal swelling, males concentrated their mating effort on females with an older infant whose maximal swelling started earlier, and they continued mating efforts until detumescence (rainmaking). These findings suggest that male bonobos distinguish between fertile and non-fertile phases of females and that having more receptive females in the party does not reduce male-male competition for fertile females.TeaserMales use the rainmaker’s rule to meet the periovulatory phase of the female bonobo for better reproductive success.

Background In temperate regions many small mammals including bats hibernate during winter. During hibernation these small mammals occasionally wake up (arouse) to restore electrolyte and water balance. However, field data on water stress and concentration of bodily fluids during hibernation is scarce. Urinary creatinine concentration has long been used to calibrate urinary hormone concentration due to its close correlation with urine concentration. Therefore, by investigating urinary creatinine concentration, we can estimate bodily fluid concentration. In this study, we investigated changes in urinary creatinine from greater horseshoe bats (Rhinolophus ferrumequinum) hibernating in abandoned mineshafts in two regions in South Korea. Results We collected 74 urine samples from hibernating greater horseshoe bats from 2018 to 2019. We found that urinary creatinine concentration was higher in February and March and then declined in April. There were also indications of a sex difference in the pattern of change in creatinine concentration over the three months. Bats in the warmer and less humid mineshaft had higher urinary creatinine concentrations than bats in the colder and more humid mineshaft. Conclusions These results indicate that hibernating bats face water stress as urinary concentration increases during winter and that water stress may vary depending on the microenvironment. Sex differences in behaviour during hibernation may influence arousal frequency and result in sex differences in changes in urinary creatinine concentration as hibernation progresses. Although further behavioural and endocrinal investigations are needed, our study suggests that urinary creatinine concentration can be used as a proxy to estimate the hydration status of bats and the effect of sex and environmental factors on arousal patterns during hibernation.

Additional file 1: Figure S1. Daily ambient temperature, TA (a) and relative humidity, RH (b) of A1 and H1 in 2019. Figure S2. Ambient temperature (top) and relative humidity (bottom) at the nearest weather stations in Cheonan (CA) and Yeonggwang (YG) in 2018 and 2019. The nearest weather station to A1 (Anseong) is 17.6km away in Cheonan (N36°45’45.576” E127°17’33.071), and for H1 (Hampyeong), it is 18.2km away in Yeonggwang (N35°17’1.932” E126°28’39.071”). Temperature data were collected by the automatic weather system (AWS) managed by the Korean Government ( https://data.kma.go.kr/ ). Figure S3. Creatinine concentrations in 2018 and 2019 (N = 74). Lines in boxes: the median, the top and bottom of boxes: the first and third quartiles, dots: creatinine concentration of each urine from females (circle) and males (triangle).

Intergroup interactions in primates vary from nonagonistic to severely aggressive. Food resources and fertile females cause intergroup aggression when groups defend resources and mates from other groups. Peaceful intermingling during intergroup encounters is rare but has been reported in several primates, including bonobos (Pan paniscus). Although intergroup encounters in bonobos occur at both nonprovisioned and provisioned sites, provisioning may be one factor responsible for frequent intergroup encounters. We studied intergroup encounters between one bonobo group (PE) and its neighboring groups, one semihabituated and two habituated groups, under nonprovisioned conditions in 2010–2015 at Wamba, Democratic Republic of Congo. We examined whether fruit abundance and females with sexual swellings influenced encounter frequency. PE group encountered the other groups on 7.1 days (mean, range: 0–19) per month. Up to four different groups met simultaneously at one location. Encounter frequency was highest around the yearly peak in fruit abundance, suggesting that reduced food competition is linked to increased encounter frequency. During periods of relatively low fruit abundance, the probability of an encounter was higher when a higher number of adult females with maximum sexual swellings were present, suggesting that the attractiveness of females with sexual swellings promoted group encounters during periods of relatively low fruit abundance. These findings suggest that both competition for food and the availability of females with sexual swellings influence encounter frequency in bonobos.

We have determined the second mitochondrial genome of Myotis bombinus Thomas, 1906 in mainland of Korea. The circular mitogenome of M. bombinus is 17,035 bp long which is slightly shorter than that of the previous mitogenome of M. bombinus. It includes 13 protein-coding genes (PCGs), two ribosomal RNA genes, and 22 transfer RNAs. The base composition was AT-biased (66.1%). Fifty single nucleotide polymorphisms and 14 insertions were identified between two mitogenomes of M. bombinus. Phylogenetic trees show that both M. bominus mitogenomes are clustered in one clade.

Infectious diseases constitute one of the major threats to African great apes. Bonobos (Pan paniscus) may be particularly vulnerable to the transmission of infectious diseases because of their cohesive grouping and frequent social and sexual interactions between groups. Here we report two cases of a flu-like illness and possible transmission of the illness among neighboring wild bonobo groups at Wamba, DR Congo. The first flu-like outbreak started in the PE group on July 28, 2013, 2 days after they had encounters with the BI and PW groups. All PE members, except for one infant, subsequently developed flu-like symptoms, including coughing and running nose. The second flu-like outbreak occurred in the E1 group on October 14, 2013, after E1 had encountered the PE group and the two groups stayed together from October 7 to 11. Eleven out of the 15 observed party members developed symptoms over the next 4 days. The pathogens underlying the two outbreaks may have been related as two temporary immigrant females, who had previously shown symptoms while in the PE group, stayed briefly in the E1 group during the second outbreak, but did not show any symptoms.

Mothers are the most fundamental individuals for the survival and development of their immature offspring. Sex-biased dispersal has an effect on strong and long-lasting social bonding between mothers and their philopatric offspring. Nepotistic relationships are often seen in species with male-biased dispersal but less frequently in species with female-biased dispersal. Bonobos are unique among female-biased dispersal primates in that the females are codominant with males, exert influence on the mating opportunities of their mature sons, and tolerate each other regardless of relatedness. Few studies on bonobos have examined sex differences in social relationships between juveniles and their mothers, and how this relates to mother-son and female-female cooperative relationships amongst adults. We investigated whether the association index of juveniles with their mothers changed with age depending on the sex of the juveniles in parties of bonobos at Wamba, the Democratic Republic of the Congo. We found that female bonobos had decreased party associations with their mothers prior to their emigration from the natal group, while male bonobos maintained relatively high party associations with their mothers. These results indicate that sex differences that emerge during the juvenile period in bonobos in their spatial relationships with their mothers differ from previous findings on chimpanzees, spider monkeys, and muriquis, in which philopatric sons tend to spend less time in proximity to their mothers and disperse earlier than, or at a similar age to, daughters. The contrasts between bonobos and other primate species suggest that the high social status of female bonobos relative to that of males may facilitate the extension of maternal support for their philopatric sons, and that high tolerance among unrelated females may enable the spatial independence of daughters from their mothers at an earlier stage.

Perineal sexual skin swelling in relation to menstrual cycle occurs in a variety of primate taxa. However, sexual swelling with exaggerated size and colour is found only in some Old World monkeys and the two Pan species. Although several hypotheses have been proposed (e.g., reliable indicator hypothesis and graded signal hypothesis), it seems unlikely that a single explanation can account for the significance of the sexual swelling in all of these species. Bonobos (Pan paniscus) provide an excellent opportunity for studying sexual swelling since they have the most prolonged maximal swelling periods among primates. In this study we propose a new hypothesis that sexual swelling in female bonobos increases their attractiveness to other females and thereby facilitates affiliative social interaction with them. We found that free-ranging female bonobos with maximal sexual swelling engaged in affiliative social interactions with other females, including genito-genital rubbing, staying in close proximity and grooming, more frequently than females without maximal swelling. These tendencies suggest that females with maximal swelling were attractive to other females. The results also suggest that the benefits of maximal swelling might vary among females depending on their life-history stage. In particular, young females may get more benefits from prolonged maximal swelling through increased grooming reciprocity and staying in close proximity to other females. Thus our study supported the hypothesis that one function of prolonged maximal swelling in bonobos is to increase attractiveness to other females, thereby enhancing affiliative relationships between females in a male-philopatric social system.

One of the most conspicuous behavioural differences among great apes is the paucity of tool use among wild bonobos (Pan paniscus) in comparison to chimpanzees (Pan troglodytes) who are one of the most prolific and skilled tool users in the animal kingdom. This is in spite of the fact that bonobo tool use repertories are as large and diverse as chimpanzees’ in captive settings. In this study, we compared tool using behaviours and potential drivers of these behaviours in the Wamba bonobo population located in central Democratic Republic of Congo with the Goualougo chimpanzee population of northern Republic of Congo. The tool use repertoire of wild bonobos was comprised of only 13 behaviours, compared to 42 for chimpanzees. However, the number of tool behaviours observed in each study site was similar between bonobos and chimpanzees, and many types of tool use for social, self-grooming/stimulation, and comfort/protection functions were commonly used by both species. A marked difference is that 25 of 42 tool behaviours exhibited by chimpanzees are performed for feeding, in contrast to a single report of bonobos using a leaf sponge to drink water. We examined whether the differences in tool use repertoires can be explained by the necessity, opportunity, relative profitability, or invention hypotheses. We found that habitat composition and fluctuation of fruit production at these two sites were similar, particularly when compared with variation observed between sites within each species. Thus it was unlikely that the necessity hypothesis explains the lack of tool use for feeding in bonobos. Though further study at Wamba is needed, we did not identify any obvious differences in prey availability that would indicate differences in tool using opportunities between the sites. This study could not test the relative profitability hypothesis, and further research is needed on whether tool use is the most efficient means of calorie or protein intake for wild apes. Bonobos at Wamba formed much larger and stable parties than chimpanzees at Goualougo, which was contrary to the prediction by the invention hypothesis. Another explanation is that differences in tool use behaviour between bonobos and chimpanzees might not be explained by the current ecological or social conditions, but rather by circumstances during the Pleistocene Epoch. The observed species differences might also reflect divergent behavioural predispositions, rather than actual differences in cognitive abilities.

Androgen receptor gene (AR), monoamine oxidase A gene (MAOA) and monoamine oxidase B gene (MAOB) have been found to have associations with behavioral traits, such as aggressiveness, and disorders in humans. However, the extent to which similar genetic effects might influence the behavior of wild apes is unclear. We examined the loci AR glutamine repeat (ARQ), AR glycine repeat (ARG), MAOA intron 2 dinucleotide repeat (MAin2) and MAOB intron 2 dinucleotide repeat (MBin2) in 32 wild bonobos, Pan paniscus, and compared them with those of chimpanzees, Pan troglodytes, and humans. We found that bonobos were polymorphic on the four loci examined. Both loci MAin2 and MBin2 in bonobos showed a higher diversity than in chimpanzees. Because monoamine oxidase influences aggressiveness, the differences between the polymorphisms of MAin2 and MBin2 in bonobos and chimpanzees may be associated with the differences in aggression between the two species. In order to understand the evolution of these loci and AR, MAOA and MAOB in humans and non-human primates, it would be useful to conduct future studies focusing on the potential association between aggressiveness, and other personality traits, and polymorphisms documented in bonobos.

Summary Some scientists have suggested that, among Hominidae, prolonged postmenopausal longevity evolved uniquely in humans [1], while others disagree [2]. There have, however, been few empirical studies on how physiological aging and somatic durability in humans compare to our closest relatives — chimpanzees and bonobos [3]. If prolonged lifespan is selected for in humans, physiological aging, including reproductive and somatic senescence, might be different for Pan and Homo . But it seems that the parameters of reproductive senescence, such as the age of having their final offspring and the number of years between generations, are not very different between chimpanzee and human females [4]. Here, we report evidence for five cases of long-sightedness (presbyopia) in old wild bonobos, exhibited during grooming. Our results suggest that senescence of the eye has not changed much since the divergence of Pan and Homo from their common ancestor.

Animals living on upper intertidal mudflats experience habitat desiccation during neap tides when water does not flood the habitat. Individuals of the manicure crab Cleistostoma dilatatum construct cone-shaped towers at the entrance of their burrows, in which they remain during neap tides. These towers are the tallest known structures compared to body size built by crabs living on intertidal flats. The frequency of tower construction followed semilunar tidal cycles with most building done prior to neap tides when few crabs were active on the mudflat surface. Bigger crabs tended to make taller and wider towers with a wider pinhole on the top. These towers may regulate the microclimate in burrows.

International audience; This paper first reviews data collected from 1976 to 2013 regarding the life histories of members of the main E1 study group of bonobos (Pan paniscus) in Wamba. The E1 group exhibited strong tendencies toward female dispersal and male residence during the entire study period, thereby exemplifying the typical characteristics of a male-philopatric and female-dispersal society. This pattern did not change after the abandonment of artificial provisioning. We then present two new cases of immigrant females, focusing especially on social association patterns, dominance relationships, and affiliative interactions during the approximate 2.5 years from the time of their immigration to their first birth. These females began engaging in social grooming with resident females immediately after their arrival but rarely did so with adult males, suggesting that they regard social bonding with females as more important than that with males. They also emigrated at a young age and frequently engaged in social play. Indeed, social bonding established through frequent social play may be related to the development of socially symmetrical relationships, which are the basis for the egalitarian bonobo society. Intragroup competition for food and mates was unlikely explanations for the tendency toward female dispersal. However, male residence and the risk of father–daughter incest may encourage female transfer among bonobos

Chimpanzees and bonobos are the closest living relatives of humans and diverged relatively recently in their phylogenetic history. However, a number of reports have suggested behavioral discrepancies between the two Pan species, such as more cooperative and tolerant social interaction and poorer tool-using repertoires in bonobos. Concerning hunting behavior and meat consumption, recent studies from the field have confirmed both behaviors not only in chimpanzees but also in bonobos. The present study reports an encounter by wild bonobos at Wamba with a duiker trapped in a snare. Bonobos interacted with the live duiker for about 10 min but did not eventually kill the animal. They showed fear responses when the duiker moved and exhibited behaviors related to anxiety and stress such as branch-drag displays and self-scratching. Although bonobos manipulated nearby saplings and parts of the snare, they did not use detached objects to make indirect contact with the duiker. Juveniles and adults of both sexes engaged in active interactions with the trapped duiker. Overall, bonobos’ behavioral responses indicated species-specific cognitive characteristics largely different from those of chimpanzees.