Social tension after grooming in wild Japanese macaques (Macaca fuscata yakui) is sex specific and sensitive to social relationships.

Changes in the rate of self-directed behavior-a proxy for social tension-offer valuable insights into individuals' experiences of social interactions. Many studies have tested the tension-reduction hypothesis, whereby grooming is expected to reduce social tension in the grooming partners. However, it is still unclear whether responses to grooming are affected by social factors such as an individual's role or social relationship with their partner, and whether responses are similar for females and males. Focussing on same-sex grooming in Yakushima Japanese macaques (Macaca fuscata yakui), we analyzed the effects of two social factors on the change in the rate of self-scratching after receiving grooming: sitting in contact with their partner outside of grooming contexts (as a measure of relationship strength) and rank distance. We collected 10-min postgrooming and matched-control focal samples on recipients of grooming. After controlling for postinhibitory rebound effects, grooming reduced scratching in females (suggesting that grooming was relaxing for the receiver), but not in males. In females, this reduction was associated with increased sitting in contact and increased rank distance: being groomed was more tension-reducing if the grooming partners spent time together outside of grooming contexts, or if their difference in rank was greater and therefore more conspicuous. The reduction effect was mediated by sitting in contact only when females had a higher-ranking-that is, more dominant and potentially aggressive-groomer. Our findings suggest that not all grooming interactions are perceived as equal, which has implications for its use as an index of relationship quality. To our knowledge, this represents the first study of postgrooming social tension in male Japanese macaques and our results highlight the need for caution when generalizing findings from only one sex to the species level.

Highly homologous simian T-cell leukemia virus type 1 genome in Japanese macaques: a large cohort study.

BACKGROUND: Simian T-cell leukemia virus type 1 (STLV-1) is a retrovirus closely related to human T-cell leukemia virus type 1 (HTLV-1), the causative agent of adult T-cell leukemia (ATL). It has been shown that Japanese macaques (Macaca fuscata, JMs) are one of the main hosts of STLV-1 and that a high percentage of JMs (up to 60%) are infected with STLV-1; however, the molecular epidemiology of STLV-1 in JMs has not been examined. METHODS: In this study, we analyzed full-length STLV-1 genome sequences obtained from 5 independent troops including a total of 68 JMs. RESULTS: The overall nucleotide heterogeneity was 4.7%, and the heterogeneity among the troops was 2.1%, irrespective of the formation of distinct subclusters in each troop. Moreover, the heterogeneity within each troop was extremely low (>99% genome homology) compared with cases of STLV-1 in African non-human primates as well as humans. It was previously reported that frequent G-to-A single-nucleotide variants (SNVs) occur in HTLV-1 proviral genomes in both ATL patients and HTLV-1 carriers, and that a G-to-A hypermutation is associated with the cellular antiviral restriction factor, Apobec3G. Surprisingly, these SNVs were scarcely observed in the STLV-1 genomes in JMs. CONCLUSIONS: Taken together, these results indicate that STLV-1 genomes in JMs are highly homologous, at least in part due to the lack of Apobec3G-dependent G-to-A hypermutation.

Examining infantile facial features and their influence on caretaking behaviors in free-ranging Japanese macaques (Macaca fuscata).

Facial features of immature individuals play a pivotal role in eliciting caretaking behaviors in humans. It has been posited that non-human animals share particular infantile facial features with humans, which can elicit caregivers' attention and caretaking behaviors. Nevertheless, the empirical examination of this hypothesis is extremely limited. In this study, we investigated infantile facial features in Japanese macaques (Macaca fuscata), their developmental processes, and their correlation with caretaking and infant behaviors, based on 470 facial photographs from one free-ranging group. We measured the size of facial parts and evaluated these features using non-contact procedures with the animals. The results indicated that, although some partial species differences were observed, the infantile facial features in Japanese macaques were broadly consistent with those previously observed in humans and great apes. Furthermore, half of the infant subjects displayed non-linear developmental trajectories of infantile faces, similar to those suggested in humans. However, unlike previous studies in humans, infantile faces were not significantly associated with maternal or non-maternal caretaking behaviors, nor were their developmental changes correlated with infant behavioral development. These findings indicate that while many aspects of infantile facial features are shared among particular primates, humans may have evolved a uniquely elevated preference for selecting such features among the primate lineage.

Deep learning for automatic facial detection and recognition in Japanese macaques: illuminating social networks.

Individual identification plays a pivotal role in ecology and ethology, notably as a tool for complex social structures understanding. However, traditional identification methods often involve invasive physical tags and can prove both disruptive for animals and time-intensive for researchers. In recent years, the integration of deep learning in research has offered new methodological perspectives through the automatisation of complex tasks. Harnessing object detection and recognition technologies is increasingly used by researchers to achieve identification on video footage. This study represents a preliminary exploration into the development of a non-invasive tool for face detection and individual identification of Japanese macaques (Macaca fuscata) through deep learning. The ultimate goal of this research is, using identification done on the dataset, to automatically generate a social network representation of the studied population. The current main results are promising: (i) the creation of a Japanese macaques' face detector (Faster-RCNN model), reaching an accuracy of 82.2% and (ii) the creation of an individual recogniser for the Kojima Island macaque population (YOLOv8n model), reaching an accuracy of 83%. We also created a Kojima population social network by traditional methods, based on co-occurrences on videos. Thus, we provide a benchmark against which the automatically generated network will be assessed for reliability. These preliminary results are a testament to the potential of this approach to provide the scientific community with a tool for tracking individuals and social network studies in Japanese macaques.

Genomic properties of a Bartonella quintana strain from Japanese macaque (Macaca fuscata) revealed by genome comparison with human and rhesus macaque strains.

Bartonella quintana, the causative agent of trench fever, is an intracellular bacterium that infects human erythrocytes and vascular endothelial cells. For many years, humans were considered the only natural hosts for B. quintana; however, it was recently discovered that wild Japanese macaques (Macaca fuscata) also serve as hosts for B. quintana. To elucidate the genetic characteristics of the B. quintana strain MF1-1 isolated from a Japanese macaque, we determined the complete genome sequence of the strain and compared it with those of strain Toulouse from a human and strain RM-11 from a rhesus macaque. General genomic features and orthologous gene cluster profiles are similar among the three strains, and strain MF1-1 is genetically closer to strain RM-11 than strain Toulouse based on the average nucleotide identity values; however, a significant inversion of approximately 0.68 Mb was detected in the chromosome of strain MF1-1. Moreover, the Japanese macaque strains lacked the bepA gene, which is responsible for anti-apoptotic function, and the trwL2, trwL4, and trwL6 genes, which may be involved in adhesion to erythrocytes of rhesus macaque and human. These features likely represent the genomic traits acquired by Japanese macaque strains in their host-associated evolution.

Metacognition in Japanese macaques (Macaca fuscata): does impulsivity explain unnecessary looks in the tubes task?

Potential metacognitive abilities, such as monitoring and controlling cognitive processes, have been revealed in some primate species. In the tubes task, apes and macaques showed higher content-checking behavior when unaware of a reward's location, but they also periodically inspected the tubes when aware, especially when a more appealing reward was involved. Some attribute this to the pleasure of looking at the reward. This study investigates whether the unnecessary tube-checking behavior observed in nine wild Japanese macaques, previously tested for metacognition using the tubes task, can be solely attributed to impulsivity. The macaques' propensity to look inside a single tube containing food they cannot immediately reach was measured and compared to their behavior in the tubes task. Results indicated that looking inside the baited tube increased as reward quality improved. However, macaques displaying unnecessary tube inspections in metacognitive tests showed less impulsivity to look. This intriguing result counters the notion that excessive looking in the tubes task is solely due to impulsive looking, prompting us to advocate for further research into the relationship between inhibition and metacognitive performance.

Decline in the Conception Rate of Wild Japanese Monkeys after the Fukushima Daiichi Nuclear Power Plant Accident.

We examined the conception rate of wild Japanese monkeys (Macaca fuscata) in Fukushima City that were exposed to radiation as a result of the Fukushima Daiichi Nuclear Power Plant accident in March 2011. The conception rate in the year of delivery from 2009 to 2022 was estimated by dissecting individuals that were euthanized by the government for population control as a countermeasure against crop damage. To evaluate the effects of exposure, the cumulative exposure dose for each individual was calculated using the concentration of radiocesium deposited in the soil at the capture site and the concentration of radiocesium in muscle estimated from the aggregated transfer factor. There were no significant differences in conception rates across all age classes over time. In terms of conception rates by age class, there was a significant decrease post-exposure compared with pre-exposure in the age class ≥ 8 years, but no significant differences in the age class 5-7 years. The non-ovulation rate did not significantly differ between the pre- and post-exposure periods for any age class. Body fat index, which can affect fertility, was compared between the pre- and post-exposure periods, and no significant differences were found in either age class. In contrast, the median total cumulative exposure (cumulative internal exposure + cumulative external exposure) was significantly higher in the age class ≥ 8 years compared with the age class 5-7 years. These results suggest that the total cumulative exposure dose may be one of the reasons for the lower conception rate in the post-exposure period among the age class ≥ 8 years.

Metacognition in wild Japanese macaques: cost and stakes influencing information-seeking behavior.

Metacognition allows us to evaluate memories and knowledge, thus enabling us to distinguish between what we know and what we do not. Studies have shown that species other than humans may possess similar abilities. However, the number of species tested was limited. Testing ten free-ranging Japanese macaques (Macaca fuscata) on a task in which they had to find food hidden inside one of the four opaque tubes, we investigated whether these subjects would seek information when needed. The monkeys could look inside the tubes before selecting one. We varied three parameters: the baiting process, the cost that monkeys had to pay to look inside the tubes, and the reward at stake. We assessed whether and how these parameters would affect the monkeys' tendency to look inside the tube before selecting one. When they were not shown which tube contained the reward, nine monkeys looked significantly more frequently in at least one condition. Half of them tended to reduce their looks when the cost was high, but only when they already knew the location of the reward. When a high-quality reward was at stake, four monkeys tended to look more inside the tubes, even though they already knew the reward's location. Our results are consistent with those of rhesus macaques, suggesting that metacognitive-like abilities may be shared by Cercopithecidae, and that, at least some monkeys may be aware of their lack of knowledge.

Automatic identification of stone-handling behaviour in Japanese macaques using LabGym artificial intelligence.

The latest advances in artificial intelligence technology have opened doors to the video analysis of complex behaviours. In light of this, ethologists are actively exploring the potential of these innovations to streamline the time-intensive behavioural analysis process using video data. Several tools have been developed for this purpose in primatology in the past decade. Nonetheless, each tool grapples with technical constraints. To address these limitations, we have established a comprehensive protocol designed to harness the capabilities of a cutting-edge artificial intelligence-assisted software, LabGym. The primary objective of this study was to evaluate the suitability of LabGym for the analysis of primate behaviour, focusing on Japanese macaques as our model subjects. First, we developed a model that accurately detects Japanese macaques, allowing us to analyse their actions using LabGym. Our behavioural analysis model succeeded in recognising stone-handling-like behaviours on video. However, the absence of quantitative data within the specified time frame limits the ability of our study to draw definitive conclusions regarding the quality of the behavioural analysis. Nevertheless, to the best of our knowledge, this study represents the first instance of applying the LabGym tool specifically for the analysis of primate behaviours, with our model focusing on the automated recognition and categorisation of specific behaviours in Japanese macaques. It lays the groundwork for future research in this promising field to complexify our model using the latest version of LabGym and associated tools, such as multi-class detection and interactive behaviour analysis.

Differential leg and trunk operation during skipping without and with hurdles in bipedal Japanese macaque.

When locomoting bipedally at higher speeds, macaques preferred unilateral skipping (galloping). The same skipping pattern was maintained while hurdling across two low obstacles at the distance of a stride within our experimental track. The present study investigated leg and trunk joint rotations and leg joint moments, with the aim of clarifying the differential leg and trunk operation during skipping in bipedal macaques. Especially at the hip, the range of joint rotation and extension at lift off was larger in the leading than in the trailing leg. The flexing knee absorbed energy and the extending ankle generated work during each step. The trunk showed only minor deviations from symmetry. Hurdling amplified the differences and notably resulted in a quasi-elastic use of the leading knee and in an asymmetric operation of the trunk.

Deep Learning for Face Detection and Pain Assessment in Japanese macaques (Macaca fuscata).

Facial expressions have increasingly been used to assess emotional states in mammals. The recognition of pain in research animals is essential for their well-being and leads to more reliable research outcomes. Automating this process could contribute to early pain diagnosis and treatment. Artificial neural networks have become a popular option for image classification tasks in recent years due to the development of deep learning. In this study, we investigated the ability of a deep learning model to detect pain in Japanese macaques based on their facial expression. Thirty to 60 min of video footage from Japanese macaques undergoing laparotomy was used in the study. Macaques were recorded undisturbed in their cages before surgery (No Pain) and one day after the surgery before scheduled analgesia (Pain). Videos were processed for facial detection and image extraction with the algorithms RetinaFace (adding a bounding box around the face for image extraction) or Mask R-CNN (contouring the face for extraction). ResNet50 used 75% of the images to train systems; the other 25% were used for testing. Test accuracy varied from 48 to 54% after box extraction. The low accuracy of classification after box extraction was likely due to the incorporation of features that were not relevant for pain (for example, background, illumination, skin color, or objects in the enclosure). However, using contour extraction, preprocessing the images, and fine-tuning, the network resulted in 64% appropriate generalization. These results suggest that Mask R-CNN can be used for facial feature extractions and that the performance of the classifying model is relatively accurate for nonannotated single-frame images.

Phylogeography and demographic history of macaques, fascicularis species group, in East Asia: Inferred from multiple genomic markers.

Climate changes at larger scales have influenced dispersal and range shifts of many taxa in East Asia. The fascicularis species group of macaques is composed of four species and is widely distributed in Southeast and East Asia. However, its phylogeography and demographic histories are currently poorly understood. Herein, we assembled autosomal, mitogenome, and Y-chromosome data for 106 individuals, and combined them with 174 mtDNA dloop haplotypes of this species group, with particular focus on the demographic histories and dispersal routes of Macaca fuscata, M. cyclopis, and M. mulatta. The results showed: (1) three monophyletic clades for M. fuscata, M. cyclopis, and M. mulatta based on the multiple genomics analyses; (2) the disparate demographic trajectories of the three species after their split ∼1.0 Ma revealed that M. cyclopis and M. fuscata were derived from an ancestral M. mulatta population; (3) the speciation time of M. cyclopis was later than that of M. fuscata, and their divergence time occurred at the beginning of "Ryukyu Coral Sea Stage" (1.0-0.2 Ma) when the East China Sea land bridge was completely submerged by the sea level rose; and (4) the three parallel rivers (Nujiang, Lancangjiang, and Jinshajiang) of Southwestern China divided M. mulatta into Indian and Chinese genetic populations ∼200 kya. These results shed light on understanding not only the evolutionary history of the fascicularis species group but also the formation mechanism of faunal diversity in East Asia during the Pleistocene.

Excess prenatal loss and respiratory illnesses of infant macaques living outdoors and exposed to wildfire smoke.

Global climate change has transformed predictions of fire seasons in the near future, and record-breaking wildfire events have had catastrophic consequences in recent years. In September 2020, multiple wildfires subjected Oregon to hazardous air quality for several days. In this retrospective cohort study, we aimed to examine prenatal loss, morbidity, and mortality of rhesus (Macaca mulatta) and Japanese macaques (Macaca fuscata) exposed to poor air quality from the nearby wildfires. Detailed medical records from 2014 to 2020 of 580 macaques housed outdoors at a research facility in Beaverton, Oregon were used to evaluate the association between these health outcomes and wildfire smoke exposure. Logistic regression models estimated excess prenatal loss, hospitalization rates, respiratory problems, and mortality during and following the wildfire event, and Kruskal-Wallis statistics were used to determine if infant growth was affected by wildfire smoke exposure. Risk of pregnancy loss (relative risk = 4.1; p < 0.001) and odds of diagnosis with a respiratory problem (odds ratio = 4.47; p = 0.003) were higher in exposed infant macaques compared to nonexposed infants. Infant growth was not affected by poor air quality exposure. Our findings suggest wildfire smoke exposure poses a risk to the health of infants and pregnant individuals and should be monitored more closely in the future.

Intense Body Contact Increases Homosexual Pair Bond Stability in Female Japanese Macaques (Macaca fuscata).

The Japanese macaque (Macaca fuscata) has become a key species for studying homosexual behavior over recent decades. With the non-conceptive nature, their same-sex consortships illustrate that individual partner preferences can exist beyond direct reproductive benefits or apparent sociosexual strategies. An open question is whether the behavior shared between partners in consortship directly affects their choice to remain with a partner. With this study, we examined behavioral aspects underlying consortship temporal patterns in these promiscuous and bisexual primates. While these patterns could be relevant in both homo- and heterosexual consortships, our study primarily focused on female-female pairs. We hypothesized that the stability of consortships (duration and occurrence) is influenced by a pair's sexual behavior, mutual sexual stimulation, and close affiliative inter-mount behaviors involving high-intensity body contact. A semi-free population of Japanese macaques was observed over one mating season. In total, 40 h of focal data on female-female consortship behaviors were analyzed. Forty-six percent of all sexually mature females engaged in homosexual interactions. Our behavioral analyses of female-female pairs found that close body contact, rather than grooming or sexual interactions, was correlated with the stability of homosexual consortships. The greater the amount of huddling and embracing a pair engaged in, the more likely they were to stay together and reunite again. However, the frequency of mounting, rubbing or thrusting had no discernable effect on consortship stability. The results of this study thus add important knowledge to partner qualities in promiscuous primates as well as to inter-group differences of homosexual behavior in Japanese macaques.

Dopamine regulates attitude toward risk.

Specific brain pathways can lower or raise the willingness of monkeys to take risks.

Balancing risk-return decisions by manipulating the mesofrontal circuits in primates.

Decision-making is always coupled with some level of risk, with more pathological forms of risk-taking decisions manifesting as gambling disorders. In macaque monkeys trained in a high risk-high return (HH) versus low risk-low return (LL) choice task, we found that the reversible pharmacological inactivation of ventral Brodmann area 6 (area 6V) impaired the risk dependency of decision-making. Selective optogenetic activation of the mesofrontal pathway from the ventral tegmental area (VTA) to the ventral aspect of 6V resulted in stronger preference for HH, whereas activation of the pathway from the VTA to the dorsal aspect of 6V led to LL preference. Finally, computational decoding captured the modulations of behavioral preference. Our results suggest that VTA inputs to area 6V determine the decision balance between HH and LL.

Perinatal Western-style diet exposure associated with decreased microglial counts throughout the arcuate nucleus of the hypothalamus in Japanese macaques.

Perinatal exposure to a high-fat, high-sugar Western-style diet (WSD) is associated with altered neural circuitry in the melanocortin system. This association may have an underlying inflammatory component, as consumption of a WSD during pregnancy can lead to an elevated inflammatory environment. Our group previously demonstrated that prenatal WSD exposure was associated with increased markers of inflammation in the placenta and fetal hypothalamus in Japanese macaques. In this follow-up study, we sought to determine whether this heightened inflammatory state persisted into the postnatal period, as prenatal exposure to inflammation has been shown to reprogram offspring immune function and long-term neuroinflammation would present a potential means for prolonged disruptions to microglia-mediated neuronal circuit formation. Neuroinflammation was approximated in 1-yr-old offspring by counting resident microglia and peripherally derived macrophages in the region of the hypothalamus examined in the fetal study, the arcuate nucleus (ARC). Microglia and macrophages were immunofluorescently stained with their shared marker, ionized calcium-binding adapter molecule 1 (Iba1), and quantified in 11 regions along the rostral-caudal axis of the ARC. A mixed-effects model revealed main effects of perinatal diet (P = 0.011) and spatial location (P = 0.003) on Iba1-stained cell count. Perinatal WSD exposure was associated with a slight decrease in the number of Iba1-stained cells, and cells were more densely located in the center of the ARC. These findings suggest that the heightened inflammatory state experienced in utero does not persist postnatally. This inflammatory response trajectory could have important implications for understanding how neurodevelopmental disorders progress.NEW & NOTEWORTHY Prenatal Western-style diet exposure is associated with increased microglial activity in utero. However, we found a potentially neuroprotective reduction in microglia count during early postnatal development. This trajectory could inform the timing of disruptions to microglia-mediated neuronal circuit formation. Additionally, this is the first study in juvenile macaques to characterize the distribution of microglia along the rostral-caudal axis of the arcuate nucleus of the hypothalamus. Nearby neuronal populations may be greater targets during inflammatory insults.

Range of rotation of thoracolumbar vertebrae in Japanese macaques.

In humans, the range of thoracic vertebral rotation is known to be greater than that of the lumbar vertebrae due to their zygapophyseal orientation and soft tissue structure. However, little is known regarding vertebral movements in non-human primate species, which are primarily quadrupedal walkers. To understand the evolutionary background of human vertebral movements, this study estimated the range of axial rotation of the thoracolumbar spine in macaque monkeys. First, computed tomography (CT) was performed while passively rotating the trunk of whole-body cadavers of Japanese macaques, after which the motion of each thoracolumbar vertebra was estimated. Second, to evaluate the influence of the shoulder girdle and surrounding soft tissues, specimens with only bones and ligaments were prepared, after which the rotation of each vertebra was estimated using an optical motion tracking system. In both conditions, the three-dimensional coordinates of each vertebra were digitized, and the axial rotational angles between adjacent vertebrae were calculated. In the whole-body condition, the lower thoracic vertebrae had a greater range of rotation than did the other regions, similar to that observed in humans. In addition, absolute values for the range of rotation were similar between humans and macaques. However, in the bone-ligament preparation condition, the upper thoracic vertebrae had a range of rotation similar to that of the lower thoracic vertebrae. Contrary to previous speculations, our results showed that the mechanical restrictions by the ribs were not as significant; rather, the shoulder girdle largely restricted the rotation of the upper thoracic vertebrae, at least, in macaques.

Age-related changes in the cranial thickness of Japanese macaques ( Macaca fuscata ) / Cambios relacionados con la edad en el grosor craneal de los macacos japoneses ( Macaca fuscata )

Craniometry has revealed that continuous skull expansion occurs after dental maturity in macaques and other nonhuman primates. Endocranial volume has been shown to increase with age from mid-adulthood to older age in macaques. Thus, neurocranial thickness may decrease with age, especially from mid-adulthood to older age. Here, we investigated age-related changes in the cranial thickness of Japanese macaques (Macaca fuscata). Ten cranial thickness measurements (ten neurocranial landmarks) were made using computed tomographic scans of 140 crania from adult macaques (67 males and 73 females). The cranial thickness at many sites was shown to increase in the neurocranium from young adulthood (7-9 years) to early-mid adulthood (14-19 years) in males and latemid adulthood (19-24 years) in females, while it was decreased in the oldest age group (>24 years). The cranial thickness at various sites showed a significant decrease from mid-adulthood to very old age in both sexes, although females had more sites with decreasing thickness than did males. The difference between sexes in terms of age-related changes in cranial thickness at sites on the mid-sagittal plane may be associated with the differences in the size of the projecting face and canines between males and females. The greater number of sites with decreasing thickness in females than in males may be associated with postmenopausal estrogen depletion in female macaques.

La craneometría ha revelado que la expansión continua del cráneo se produce después de la madurez dental en macacos y otros primates no humanos. Se ha demostrado que el volumen endocraneal aumenta con la edad desde mediados de la edad adulta hasta la edad más avanzada en macacos. Por lo tanto, el grosor neurocraneal puede disminuir con la edad, especialmente desde la edad adulta media hasta la edad avanzada. Aquí, investigamos los cambios relacionados con la edad en el grosor craneal de los macacos Japoneses (Macaca fuscata). Se realizaron diez mediciones del grosor craneal (considerando diez puntos de referencia neurocraneales) mediante tomografías computarizadas de 140 cráneos de macacos adultos (67 machos y 73 hembras). Se observó que el grosor craneal en muchos sitios aumentó en el neurocráneo desde la edad adulta joven (7-9 años) hasta la edad adulta media (14-19 años) en los hombres y en la edad adulta media tardía (19-24 años) en las mujeres, mientras que se redujo en el grupo de mayor edad (> 24 años). El grosor craneal en varios sitios mostró una disminución significativa desde la edad adulta media hasta la edad muy avanzada en ambos sexos, aunque las hembras tenían más sitios con grosor decreciente. La diferencia entre sexos, en términos de cambios relacionados con la edad, en el grosor craneal en los sitios en el plano mediano puede asociarse con las diferencias en el tamaño de la cara y en los caninos entre machos y hembras. El mayor número de sitios con grosor decreciente en las hembras respecto a los machos puede estar asociado con el agotamiento de los estrógenos posmenopáusicos en los macacos hembras.