Increased urinary creatinine during hibernation and day roosting in the Eastern bent-winged bat (Miniopterus fuliginosus) in Korea.

Torpor and arousal cycles, both daily and seasonal (e.g. hibernation), are crucial for small mammals, including bats, to maintain the energy and water balance. The alternation between torpor and arousal leads to metabolic changes, leaving traceable evidence of metabolic wastes in urine. In this study we investigated urinary creatinine and acetoacetate (a ketone body) in the Eastern bent-wing bat (Miniopterus fuliginosus) in Mungyeong, South Korea. We found an increase in urinary creatinine during torpor in summer, indicating changes in renal water reabsorption rates during the active season. Although we could not confirm ketonuria in hibernating bats due to a methodological limitation caused by the small amount of urine, we verified an increase in urinary creatinine concentration during hibernation. This finding suggests that managing water stress resulting from evaporative water loss is one of key reasons for arousal during hibernation in Eastern bent-wing bats.

The effects of visitors and social isolation from a peer on the behavior of a mixed-species pair of captive gibbons.

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 social group setting 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 separated during the study period, and we examined whether the social isolation stimulated the visitor effect. The frequency of stress-related behaviors of the gibbons increased and the social playing between them decreased proportionally to visitor number. 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. Future studies with larger sample sizes will improve the understanding of the visitor effect and the social setting in the captivity.

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.

Urinary creatinine varies with microenvironment and sex in hibernating Greater Horseshoe bats (Rhinolophus ferrumequinum) in Korea.

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.

The complete mitochondrial genome of the far Eastern myotis: Myotis bombinus Thomas, 1906 in mainland of Korea (Chiroptera, Vespertilionidae).

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.

Age and sex differences in juvenile bonobos in party associations with their mothers at Wamba.

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.

Occurrence and transmission of flu-like illness among neighboring bonobo groups at Wamba.

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.

Long-sightedness in old wild bonobos during grooming.

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.

Androgen receptor and monoamine oxidase polymorphism in wild bonobos.

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.