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.

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.

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.

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.

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.

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.

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.

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.

Distribution of P2X3 purinoceptor-immunoreactive sensory nerve endings in the carotid body of Japanese macaque (Macaca fuscata).

In the carotid body of laboratory rodents, adenosine 5'-triphosphate (ATP)-mediated transmission is regarded as critical for transmission from chemoreceptor type I cells to P2X3 purinoceptor-expressing sensory nerve endings. The present study investigated the distribution of P2X3-immunoreactive sensory nerve endings in the carotid body of the adult male Japanese monkey (Macaca fuscata) using multilabeling immunofluorescence. Immunoreactivity for P2X3 was detected in nerve endings associated with chemoreceptor type I cells immunoreactive for synaptophysin. Spherical or flattened terminal parts of P2X3-immunoreactive nerve endings were in close apposition to the perinuclear cytoplasm of synaptophysin-immunoreactive type I cells. Immunoreactivity for ectonucleoside triphosphate diphosphohydrolase 2 (NTPDase2), which hydrolyzes extracellular ATP, was localized in the cell body and cytoplasmic processes of S100B-immunoreactive cells. NTPDase2-immunoreactive cells surrounded P2X3-immunoreactive terminal parts and synaptophysin-immunoreactive type I cells, but did not intrude into attachment surfaces between terminal parts and type I cells. These results suggest ATP-mediated transmission between type I cells and sensory nerve endings in the carotid body of the Japanese monkey, as well as those of rodents.

Hybridization and its impact on the ontogenetic allometry of skulls in macaques.

The role of hybridization in morphological diversification is a fundamental topic in evolutionary biology. However, despite the accumulated knowledge on adult hybrid variation, how hybridization affects ontogenetic allometry is less well understood. Here, we investigated the effects of hybridization on postnatal ontogenetic allometry in the skulls of a putative hybrid population of introduced Taiwanese macaques (Macaca cyclopis) and native Japanese macaques (Macaca fuscata). Genomic analyses indicated that the population consisted of individuals with varying degrees of admixture, formed by male migration from Japanese to Taiwanese macaques. For overall skull shape, ontogenetic trajectories were shifted by hybridization in a nearly additive manner, with moderate transgressive variation observed throughout development. In contrast, for the maxillary sinus (hollow space in the face), hybrids grew as fast as Taiwanese macaques, diverging from Japanese macaques, which showed slow growth. Consequently, adult hybrids showed a mosaic pattern, that is, the maxillary sinus is as large as that of Taiwanese macaques, while the overall skull shape is intermediate. Our findings suggest that the transgressive variation can be caused by prenatal shape modification and nonadditive inheritance on regional growth rates, highlighting the complex genetic and ontogenetic bases underlying hybridization-induced morphological diversification.

Whole-exome sequencing analysis of patent ductus arteriosus in a Japanese macaque (Macaca fuscata).

We performed whole-exome sequencing using a human exome capture kit to analyze the potential genetic factors related to patent ductus arteriosus in Japanese macaques. Compared with the reference sequences of other primates, we identified potential missense variants in five genes: ADAM15, AZGP1, CSPG4, TNFRSF13B, and EPOR.

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.

Phylogenetic analyses of Chilomastix and Retortamonas species using in vitro excysted flagellates.

In vitro excystation of cysts of microscopically identified Chilomastix mesnili and Retortamonas sp. isolated from Japanese macaques and Retortamonas sp. isolated from small Indian mongooses could be induced using an established protocol for Giardia intestinalis and subsequently by culturing with H2S-rich Robinson's medium supplemented with Desulfovibrio desulfuricans. Excystation usually began 2 h after incubation in Robinson's medium. DNA was isolated from excysted flagellates after 4 h of incubation or from cultured excysted flagellates. Phylogenetic analysis based on their 18S rRNA genes revealed that two isolates of C. mesnili from Japanese macaques belonged to the same cluster as a C. mesnili isolate from humans, whereas a mammalian Retortamonas sp. isolate from a small Indian mongoose belonged to the same cluster as that of an amphibian Retortamonas spp. isolate from a 'poison arrow frog' [sequence identity to AF439347 (94.9%)]. These results suggest that the sequence homology of the 18S rRNA gene of the two C. mesnili isolates from Japanese macaques was similar to that of humans, in addition to the morphological similarity, and Retortamonas sp. infection of the amphibian type in the small Indian mongoose highlighted the possibility of the effect of host feeding habitats.

Bioacoustic monitoring to determine addiction levels of primates to the human sphere: A feasibility study on Japanese macaques.

Some nonhuman primate species, whose original habitats have been reclaimed by artificial activities, have acquired boldness toward humans which is evident based on the diminished frequency of escape behaviors. Eventually, such species have become regular users of human settlements, and are referred to as "urban primates." Considering this, we developed a noninvasive technique based on bioacoustics to provide a transparent assessment of troop addiction levels in anthropogenic environments, which are determined by the dependence on agricultural crops and human living sphere for their diets and daily ranging, respectively. We attempted to quantify the addiction levels based on the boldness of troops when raiding settlements, characterized by a "landscape of fear" because of the presence of humans as predators. We hypothesized that the boldness of troops could be measured using two indices: the frequency of raiding events on settlements and the amount of time spent there. For hypothesis testing, we devised an efficient method to measure these two indices using sound cues (i.e., spontaneous calls) for tracing troop movements that are obtainable throughout the day from most primate species (e.g., contact calls). We conducted a feasibility study of this assessment procedure, targeting troops of Japanese macaques (Macaca fuscata). For this study, we collected 346 recording weeks of data using autonomous recorders from 24 troops with different addiction levels during the nonsnowy seasons. The results demonstrated that troops that reached the threshold level, at which radical interventions including mass culling of troop members is officially permitted, could be readily identified based on the following behavioral characteristics: troop members raiding settlements two or three times per week and mean time spent in settlements per raiding event exceeding 0.4 h. Thus, bioacoustic monitoring could become a valid option to ensure the objectivity of policy judgment in urban primate management.

A Maternal Western-Style Diet Impairs Skeletal Muscle Lipid Metabolism in Adolescent Japanese Macaques.

Maternal consumption of a Western-style diet (mWD) during pregnancy alters fatty acid metabolism and reduces insulin sensitivity in fetal skeletal muscle. The long-term impact of these fetal adaptations and the pathways underlying disordered lipid metabolism are incompletely understood. Therefore, we tested whether a mWD chronically fed to lean, insulin-sensitive adult Japanese macaques throughout pregnancy and lactation would impact skeletal muscle oxidative capacity and lipid metabolism in adolescent offspring fed a postweaning (pw) Western-style diet (WD) or control diet (CD). Although body weight was not different, retroperitoneal fat mass and subscapular skinfold thickness were significantly higher in pwWD offspring consistent with elevated fasting insulin and glucose. Maximal complex I (CI)-dependent respiration in muscle was lower in mWD offspring in the presence of fatty acids, suggesting that mWD impacts muscle integration of lipid with nonlipid oxidation. Abundance of all five oxidative phosphorylation complexes and VDAC, but not ETF/ETFDH, were reduced with mWD, partially explaining the lower respiratory capacity with lipids. Muscle triglycerides increased with pwWD; however, the fold increase in lipid saturation, 1,2-diacylglycerides, and C18 ceramide compared between pwCD and pwWD was greatest in mWD offspring. Reductions in CI abundance and VDAC correlated with reduced markers of oxidative stress, suggesting that these reductions may be an early-life adaptation to mWD to mitigate excess reactive oxygen species. Altogether, mWD, independent of maternal obesity or insulin resistance, results in sustained metabolic reprogramming in offspring muscle despite a healthy diet intervention. ARTICLE HIGHLIGHTS: In lean, active adolescent offspring, a postweaning Western-style diet (pwWD) leads to shifts in body fat distribution that are associated with poorer insulin sensitivity. Fatty acid-linked oxidative metabolism was reduced in skeletal muscles from offspring exposed to maternal Western-style diet (mWD) even when weaned to a healthy control diet for years. Reduced oxidative phosphorylation complex I-V and VDAC1 abundance partially explain decreased skeletal muscle respiration in mWD offspring. Prior exposure to mWD results in greater fold increase with pwWD in saturated lipids and bioactive lipid molecules (i.e. ceramide and sphingomyelin) associated with insulin resistance.

Estimation of external dose for wild Japanese macaques captured in Fukushima prefecture: decomposition of electron spin resonance spectrum.

The signal intensities of CO2- radicals in teeth can be utilised as an individual indicator of the cumulative external dose for animals. To accurately determine the external dose, it is desirable to analyse the CO2- radical intensity and improve its detection limit. We recently reported a dose-response in the range of 0-200 mGy and estimated the absorbed dose for seven wild Japanese macaques captured in/around the related areas to the Fukushima Daiichi Nuclear Power Plant accident. Herein, for further improvement of this method, we examined the electron spin resonance spectra of the teeth of these seven and an additional four macaques captured in Fukushima by applying two spectrum-decomposition algorithms.