Sex‐specific participation in inter‐group conflicts within a multilevel society: the first evidence at the individual level

Inter‐group conflicts are common among many group‐living animals and involve potentially complex motivations and interactions. Mammals living in multilevel societies offer a good opportunity to study inter‐group conflicts. This study is the first to explore the function of sex‐specific participation during inter‐group conflicts within a multilevel society at the individual level. The Sichuan snub‐nosed monkey (Rhinopithecus roxellana) is an endangered seasonal breeding species living in a multilevel society. From Sep 2007 to May 2008 we recorded 290 inter‐group conflicts of a free‐ranging provisioned band of R. roxellana in the Qinling Mountains of China to investigate the function of individual aggression during inter‐group encounters. Our findings show that adult males were the main participants in inter‐group conflicts, while females took part in them only occasionally. The male participation rate during the mating season, when adult females were estrous, was significantly higher than that during the non‐mating season. Furthermore, males directed their aggression to other males, and directed more intense aggression towards bachelor males than towards other resident males. For both sexes, the participation rate as initiators was higher in the winter than that in the spring; and there was a significant positive correlation between group size and the participation rate as initiators. Our results suggest that inter‐group aggression in Sichuan snub‐nosed monkeys is linked to both mate defense and resource defense.     

Invasion and defense of the basic social unit in a nonhuman primate society leads to sexual differences in the gut microbiome

Multilevel society is one of the most complex social systems in natural ecosystems and is a typical feature among some primates. Given the potential connection between social behavior and gut microbiome composition, the multilevel social system could affect the primate gut microbiome. Here, based on long-term observation (e.g. social unit dynamics, transfer, and behavior), we investigated this potential integrating 16S rRNA gene amplicon sequencing and behavior data in Yunnan snub-nosed monkeys (Rhinopithecus bieti), which possess a multilevel social group based on one male units (OMUs, each unit with several breeding females and their offspring) and all-male unit (AMU, several bachelor males residing together). We found that the mean unweighted Unifrac distance between adult males from different OMUs was significantly lower than that between adult females from different OMUs (paired Wilcoxon test, P = 0.007). There was no significant difference in the mean unweighted Unifrac distance between females within the same OMU or between females from different OMUs. These findings indicated the potential connection between the defense and invasion of social units and the gut microbiome community in wild Yunnan snub-nosed monkeys. We speculated that the resident males of OMUs displaying a significantly higher similarity in the gut microbial community than that of adult females in separate OMUs might be associated with the sexual differences in their interactions and from previously having cohabitated together in the AMU. Therefore, this study suggested that multilevel societies might have an effect on the gut microbial community in this wild nonhuman primate species.     

Substrate use and postural behavior in free‐ranging snub‐nosed monkeys (Rhinopithecus bieti) in Yunnan

Extant colobines represent a predominantly arboreal primate radiation, but there are outliers such as some species of snub‐nosed monkeys (Rhinopithecus spp.) that utilize both arboreal and terrestrial substrates. We quantified the degree of terrestriality and the distribution of individuals across canopy levels, the extrinsic and intrinsic determinants and constraints of strata association as well as use of postures in relation to behavior and food sources in a wild population of Yunnan snub‐nosed monkeys (Rhinopithecus bieti) in the Samage Forest, China. The subjects spent 80.5% of the observation time in the trees and 19.5% on the ground. Ground use occurred most frequently in the context of travelling (61%) and less often in the context of feeding and resting (30% combined). Adult males frequented the ground significantly more often than other age‐sex classes. Age‐sex differences were also apparent in substrate preferences, which likely reflect body weight constraints. Adult males were significantly more associated with solid substrates and less with terminal branches than adult females and juveniles. Juveniles were seen more often on unstable ground (i.e. on thin and oblique branches) and in the upper canopy. Substrate use also varied with behavior: feeding was much more common in the upper stratum, outer canopy, on highly inclined and thin branches, as compared to resting. Severe weather also influenced canopy use in that tree crowns were used less often during periods of snowfall. The most frequently exhibited resting and feeding postures was sitting. Standing and suspensory postures were most often used in the context of feeding on lichens.     

Foot use and hand preference during feeding in captive black‐and‐white snub‐nosed monkeys (Rhinopithecus bieti)

Postural origin theory predicts that body postures are related to hand preference in nonhuman primates due to hemispheric specialization. Foot preference, especially in manipulating objects, is also a good predictor of hemispheric specialization in humans. We studied limb (hand and foot) preferences in 11 captive adult black‐and‐white snub‐nosed monkeys (Rhinopithecus bieti) to see how limb preference is influenced by postures and foot manipulation. Hand preference was significantly different for this group between quadrupedal standing and clinging postures, and sitting and clinging postures, but not between bipedal standing and clinging postures. Individuals were significantly more likely to use the right hand in the clinging posture than in quadrupedal standing or sitting postures. In the sitting posture, individuals maintained their respective hand preference even when the food was on the other side of the body. There was a gender difference in the sitting posture, where females preferred their right hand but males preferred their left. Individuals who did not routinely use their feet to manipulate objects, compared to those who did, shifted to greater right hand use from the clinging posture to the bipedal posture. One male individual and his offspring were more likely to use their feet to manipulate objects than the rest of the monkeys. In the present study, we reveal the first evidence of a postural effect on hand preference in R. bieti as well as a foot preference in this species. Our results mostly agree with the postural origin theory and hemispheric specialization.     

Major histocompatibility complex and mate choice in the polygynous primate: the Sichuan snub‐nosed monkey (Rhinopithecus roxellana)

The highly polymorphic genes within the major histocompatibility complex (MHC) not only play a major role in immunity resistance, but also seem to provide hints for mate choice in some animal populations. In the present study we investigated MHC‐related mate choice in a small natural population (group size 40–55 individuals) of a polygynous primate, the Sichuan snub‐nosed monkey (Rhinopithecus roxellana). We found that there was no evidence either for MHC‐disassortative mating, or for females to mate with males based on MHC heterozygosity or specific alleles. Nevertheless, of the 11 alleles identified, we found that the frequencies of 2 alleles, Rhro‐DRB2 (P < 0.01) and Rhro‐DRB5 (P < 0.05) were higher in offspring than in their parents. These findings suggest that MHC‐DRB in this population of R. roxellana is unlikely to be associated with mating preferences. Limited female opportunities for mate choice are likely due, in part, to the harem breeding structure present in R. roxellana, and the relatively small number of resident adult males in our study band (N = 4–6). In addition, we suggest that differences in the frequency of particular alleles across generations may be linked to parasite resistance in a fluctuating environment; however, confirmation of this finding requires further study.     

Distribution of sleeping sites of the Yunnan snub‐nosed monkey (Rhinopithecus bieti) in the Samage Forest,China

Sleeping site locations are important to free‐ranging primate groups. Sites are strategically selected by primates so as to optimize security, comfort and foraging efficiency. Data were collected on the distribution of sleeping sites of the Yunnan snub‐nosed monkey (Rhinopithecus bieti) between Sep 2005 and Sep 2006 at Gehuaqing in Baimaxueshan Nature Reserve, China. We identified 54 sleeping sites, which were used 137 times during the study period. These sleeping sites were distributed throughout the monkey group's total home range. R. bieti preferred certain sleeping sites over others: 63% of the sleeping sites were used 2 or more times in 13 months. Groups reused locations in an unpredictable long‐term pattern, but avoided using the same sleeping site on consecutive nights. To reduce the time and energetic costs of travel, monkeys preferred sleeping near commonly used feeding sites. We recorded 124 feeding sites in the home range, which were used 174 times. A total of 27 sleeping sites were also feeding sites, and all remaining sleeping sites were close to feeding sites. There was a positive correlation between the intensity of use of sleeping sites and feeding sites. The present study suggests that the availability and the location of immediate sources of food is a key factor in the choice of sleeping sites.     

Characteristics of night‐time sleeping places selected by golden monkeys (Rhinopithecus bieti) in the Samage Forest,Baima Snow Mountain Nature Reserve,China

We examined the criteria for sleeping place selection in a social band of Rhinopithecus bieti (black‐and‐white snub‐nosed or golden monkeys) living in the mountainous Samage Forest, Baima Snow Mountain Nature Reserve, Yunnan, China. We performed principal component analysis and found that slope aspect, tree height and trunk diameter were likely key variables influencing selection of sleeping places. Sleeping sites were preferentially located in mixed deciduous/conifer forest. The monkeys slept exclusively in evergreen trees, of which 82% were conifers (mostly Picea likiangensis and Tsuga dumosa) and 18% evergreen oaks (Cyclobalanopsis oxyodon and Quercus spp.). Sleeping trees were tall (mean 30.5 m), had high boles (mean 18.4 m), large diameters (mean 62.6 cm) and large crown areas (mean 57.9 m²). A comparative analysis of phytological and architectural features between trees in “sleeping site plots” (n= 18) and trees in “non‐sleeping‐site plots” (n= 66) revealed that diameter, crown surface area and tree height were significantly (P < 0.01) larger in the former compared with the latter. All investigated roosting sites were situated on steep mountain slopes. Valleys and mountain ridges were avoided. We also detected re‐use of roosting sites on several occasions, but not on consecutive nights. It is most likely that a mix of factors (stability of trees, access to food, unit cohesion, monitoring potential) explains the pattern of sleeping site preference, but predation at night seems to be only slightly important. Climate appears to have a profound influence on patterns of sleeping site selection in the monkeys' harsh temperate habitat. This is demonstrated by the monkeys' preference for mixed forest at medium elevations over montane fir forest at high elevations and slopes instead of ridges, with reduced exposure to wind and precipitation inherent in the former. We also emphasize the possibly substantial role that non‐environmental factors (the nature of social organization and socio‐behavioral strategies) play in determining sleeping site use in R. bieti and other primates.     

Eurasian blackbird predated by wild Rhinopithecus roxellana in the Qinling Mountains,China

Although there are some reports that have described primates eating animals, it is unknown whether predation on vertebrates exists in herbivorous leaf‐eating primates. We have witnessed firsthand wild Sichuan snub‐nosed monkeys (Rhinopithecus roxellana) preying on and consuming Eurasian blackbirds (Turdus meruld) in the Qinling Mountains of China. This event suggests that R. roxellana, which has previously been described as a herbivorous leaf‐eating primate, may be partially carnivorous and the correct classification of this species would be omnivorous. Furthermore, food‐share behavior among higher‐ranked members occurs in a one‐male unit when vertebrate prey is hunted by this species.     

A short note on extractive foraging behavior in gray snub‐nosed monkeys

Extractive foraging (EF) involves the exploitation of hidden or embedded foods, generally any food that is not visible to the naked eye. Therefore, EF is particularly important for survival in marginal habitats as it provides seasonal fallback foods in low food availability seasons. Although many studies consider primates’ EF behavior and category, colobine species are usually categorized as non‐extractive foragers and few studies quantitatively examine their EF behavior. In this study, we examined the EF behavior of one colobine species, the gray snub‐nosed monkey (Rhinopithecus brelichi), at Yangaoping in Fanjingshan National Nature Reserve, Guizhou. We recorded 6 categories of EF behaviors. The most frequently sought‐out foods were seeds, young bamboo and invertebrates. Extracted foods accounted for an average of 26.02% of feeding records. As the monkey engages in little EF behavior in the winter when the food availability is low, these results seem to do not support the hypothesis that EF serves to secure additional resources during lean times in marginal or seasonal habitats. According to these findings, we suggest R. brelich should be considered as an extractive forager. Our study also highlights the need for increased representation of colobines in the EF literature to better inform the discussion concerning its link to primate brain evolution.     

Genetic analysis of group composition and relatedness in white‐headed langurs

We collected fecal samples of white‐headed langurs from 3 of the 4 remaining habitat fragments (Fa, Fb and CZ) located in southwestern Guangxi, China in Nov 2005, and used 5 microsatellite loci and the SRY gene to assess the relatedness between 46 langurs within and between groups. We observed 2 forms of group structure: one‐male/multi‐female groups (OMGs) and all‐male groups (AMGs). One AMG in Fa was composed of 2 generations, included a father, 2 sons and 1 unrelated male, and all OMGs in all 3 habitats included 1 resident male, several adult females and offspring. Of the 21 identified father‐offspring cases, the resident male fathered 20 (95%) and the non‐resident male sired 1 (5%), suggesting that adult males had overwhelming priority of access to females as the resident male in an OMG, while the non‐resident male may also have the opportunity to adopt surreptitious mating strategies.     

Using unmanned aerial vehicles with thermal‐image acquisition cameras for animal surveys: a case study on the Sichuan snub‐nosed monkey in the Qinling Mountains

Following significant developments in technology, alternative devices have been applied in fieldwork for animal and plant surveys. Thermal‐image acquisition cameras installed on unmanned aerial vehicles (UAVs) have been used in animal surveys in the wilderness. This article demonstrates an example of how UAVs can be used in high mountainous regions, presenting a case study on the Sichuan snub‐nosed monkey with a detection rate of 65.19% for positive individual identification. It also presents a model that can prospectively predict population size for a given animal species, which is based on combined initial work using UAVs and traditional surveys on the ground. A great potential advantage of UAVs is significantly shortening survey procedures, particularly for areas with high mountains and plateaus, such as the Himalayas, the Qinghai–Tibet Plateau, Hengduan Mountains, the Yunnan‐Gui Plateau and Qinling Mountains in China, where carrying out a traditional survey is extremely difficult, so that species and population surveys, particularly for critically endangered animals, are largely absent. This lack of data has impacted the management of endangered animals as well as the formulation and amendment of conservation strategies.     

Male attacks on infants and infant death during male takeovers in wild white‐headed langurs (Trachypithecus leucocephalus)

Infanticide was first observed in langurs nearly 50 years ago, and this rare phenomenon has been inferred to have either an evolutionarily adaptive function or to be a pathological and non‐functional behavior. In this study, we report 5 male takeover events in one‐male groups of white‐headed langurs in the Nongguan Karst Hills, Guangxi, China from 1998 to 2006. We recorded 13 attacks on 9 infants by extra‐group males or new resident males. During the male takeovers, all of the infants younger than 6 months (with an average age of 3.6 months [N = 11]) in the groups disappeared. The infant death rate during the 4.2 months after takeover by a new male was significantly higher than the infant death rate calculated for most of the year. Older infants that were still nursing (with an average age of 14.1 months [N = 7]) were often attacked and seriously wounded by the extra‐group males or new resident males, but all of them survived. The interbirth intervals of females whose infants were assumed to be killed by males were significantly reduced relative to those of females in groups with stable male tenure (mean = 10 months vs 25 months). Our data suggest that males kill unrelated and unweaned infants during the takeover period to decrease the time until the infants’ mothers resume fertility. Thus, infanticide would support sexual selection theory in white‐headed langurs. The data also show that infanticidal behavior was directed toward the infants, especially those who were still nursing. Female dispersal may function as a counter‐strategy to avoid infanticide.     

The Biology of Soft Shores and Estuaries

Sociality confers many benefits to gregarious animals, but group-living does not come without associated costs. Social living can cause anxiety, which if prolonged can lead to stress. We investigate correlates of anxiety and stress among wild adult male olive baboons (Papio hamadryas anubis) in Gashaka-Gumti National Park, Nigeria, and present the first examination of these correlates for male baboons living in forested environments. We used rates of self-directed behaviours (SDB) to quantify anxiety, and faecal glucocorticoid (FGC) concentrations to quantify physiological stress. We first examined the relationship between SDB rates and FGC concentrations, and then examined each measure in relation to a range of variables previously linked to anxiety or stress. We found that SDB rates and FGC concentrations were not correlated with each other, nor were they related to any measure of grooming or receiving aggression. SDB rates were negatively correlated with time spent with an adult female as nearest neighbour, but were unrelated to time with another adult male as closest conspecific. FGC concentrations were unrelated to time with adult nearest neighbours of either sex. Our results add to the growing body of literature examining the psychological and physiological costs of social living among wild primates.     

Fatal Gastrointestinal Infection with ‘Flexispira rappini’‐Like Organisms in a Cat

A 4‐month‐old male British Blue cat with catarrhal to haemorrhagic enteritis showed massive colonization of the stomach, small intestine and caecum with spiral‐shaped bacilli. In the stomach, organisms were located in foveolae and gland lumina and within unaltered and degenerate epithelial cells. Inflammatory infiltration was moderate and T cell dominated. In the intestine, bacilli were found in the gut lumen, between villi, in crypt lumina and within epithelial cells. Degeneration of crypt epithelial cells as well as crypt dilation and moderate to massive macrophage‐dominated infiltration of the mucosa and submucosa were observed. Immunohistochemically, bacilli were positive with an antibody against Helicobacter. Ultrastructurally, the organisms strongly resembled ‘Flexispira rappini’, a spiral‐shaped Helicobacter species known as a normal intestinal colonizer in dogs and mice.     

Methicillin‐resistant Staphylococcus aureus in Resident Animals of a Long‐term Care Facility

Animals provide benefits to elderly and chronically ill people by decreasing loneliness, increasing social interactions, and improving mental health. As a result, many hospitals and long‐term care facilities allow family pets to visit ill or convalescing patients or support animal‐assisted therapy programs. These include programs that have resident animals in long‐term care facilities. Despite the benefits, there are concerns about disease transmission between pets and patients. Antibiotic‐resistant bacteria, such as methicillin‐resistant Staphylococcus aureus (MRSA), are a recognized problem in healthcare settings leading to refractory infections and potentially life‐threatening illnesses. MRSA has been isolated from numerous animal species, yet few studies are available on the carriage of this pathogen in animals residing in long‐term care facilities. Our objective was to characterize MRSA carriage among resident animals in a long‐term care facility. Methods: To document MRSA colonization, nasal swabs from 12 resident animals (one dogs and 11 cats) of a long‐term care facility were collected weekly for 8 weeks. Staphylococcus isolates were characterized by antimicrobial susceptibility and MRSA isolates were further characterized by pulsed‐field gel electrophoresis (PFGE). PFGE isolate patterns were compared with an existing database of MRSA isolate patterns at the Minnesota Department of Health. Results: Two of 11 cats were colonized with MRSA. MRSA was recovered from five of eight weekly samples in one cat and two of eight weekly samples in the other cat. All isolates were classified as USA100 (healthcare‐associated strains). Discussion: Long‐term care resident animals may acquire MRSA. Clonally related strains were identified over the 8‐week sampling period. It is unclear if pets serve as an on‐going source of infection to their human companions in long‐term care facilities.     

Kisspeptin‐10 stimulates the release of luteinizing hormone and testosterone in pre‐ and post‐pubertal male goats

The aims of the present study were to clarify the effect of kisspeptin‐10 (Kp10) on the secretion of luteinizing hormone (LH) and testosterone (T) in pre‐pubertal and post‐pubertal male ruminants. Four male goats (Shiba goats) were given an intravenous (i.v.) injection of Kp10 (5 µg/kg body weight (b.w.)), gonadotoropin‐releasing hormone (GnRH, 1 µg/kg b.w.), or 2 mL of saline as a control at the ages of 3 (pre‐pubertal) and 6 (post‐pubertal) months. A single i.v. injection of Kp10 significantly stimulated the release of LH and T in both groups. The area under the response curve (AUC) of LH for a 60‐min period after the i.v. injection of Kp10 was significantly greater in the pre‐pubertal goats (P < 0.05). The AUC of T for a 120 min period post‐injection did not differ between the two age groups. A single i.v. injection of GnRH also significantly stimulated the release of LH and T in both groups (P < 0.05). The secretory pattern of LH and T in response to GnRH resembled that in response to Kp10. These results show that the LH‐releasing response to Kp10 is greater in pre‐pubertal than post‐pubertal male goats. They also show that Kp10, as well as GnRH, is able to stimulate the release of T in male goats.     

Visual landmark‐directed scatter‐hoarding of Siberian chipmunks Tamias sibiricus

Spatial memory of cached food items plays an important role in cache recovery by scatter‐hoarding animals. However, whether scatter‐hoarding animals intentionally select cache sites with respect to visual landmarks in the environment and then rely on them to recover their cached seeds for later use has not been extensively explored. Furthermore, there is a lack of evidence on whether there are sex differences in visual landmark‐based food‐hoarding behaviors in small rodents even though male and female animals exhibit different spatial abilities. In the present study, we used a scatter‐hoarding animal, the Siberian chipmunk, Tamias sibiricus to explore these questions in semi‐natural enclosures. Our results showed that T. sibiricus preferred to establish caches in the shallow pits labeled with visual landmarks (branches of Pinus sylvestris, leaves of Athyrium brevifrons and PVC tubes). In addition, visual landmarks of P. sylvestris facilitated cache recovery by T. sibiricus. We also found significant sex differences in visual landmark‐based food‐hoarding strategies in Siberian chipmunks. Males, rather than females, chipmunks tended to establish their caches with respect to the visual landmarks. Our studies show that T. sibiricus rely on visual landmarks to establish and recover their caches, and that sex differences exist in visual landmark‐based food hoarding in Siberian chipmunks.     

Foraging technique and prey‐handling time in black‐necked stork (Ephippiorhynchus asiaticus)

The foraging technique and prey‐handling time of the black‐necked stork (Ephippiorhynchus asiaticus) was studied in Dudhwa National Park, India, from January 1996 to June 1997. The habitat in which the storks foraged played an important role in selecting a particular technique to procure food. Black‐necked storks mostly foraged using a tactile technique (>90%), but sometimes foraged visually. When the water level was estimated to be less than 60 cm, the storks foraged using tactile techniques. There was no difference in the feeding techniques of male and female storks. Foraging attempt rates varied between the sexes in summer (May) and during late winter (February) in 1997. The search time for prey increased when the water level was high and fish were widely distributed. Decreases in water level resulted in concentration offish in certain areas and this contributed to high fish‐catching rates by black‐necked storks. Males had a higher success rate offish capture than females. However, females captured longer fish than males. Prey‐handling time increased in both sexes as fish length increased. Fish 4–6 cm long were most frequently taken by the foraging storks.     

Unknown‐parent groups in single‐step genomic evaluation

In single‐step genomic evaluation using best linear unbiased prediction (ssGBLUP), genomic predictions are calculated with a relationship matrix that combines pedigree and genomic information. For missing pedigrees, unknown selection processes, or inclusion of several populations, a BLUP model can include unknown‐parent groups (UPG) in the animal effect. For ssGBLUP, UPG equations also involve contributions from genomic relationships. When those contributions are ignored, UPG solutions and genetic predictions can be biased. Options to eliminate or reduce such bias are presented. First, mixed model equations can be modified to include contributions to UPG elements from genomic relationships (greater software complexity). Second, UPG can be implemented as separate effects (higher cost of computing and data processing). Third, contributions can be ignored when they are relatively small, but they may be small only after refinements to UPG definitions. Fourth, contributions may approximately cancel out when genomic and pedigree relationships are constructed for compatibility; however, different construction steps are required for unknown parents from the same or different populations. Finally, an additional polygenic effect that also includes UPG can be added to the model.