Macaca Fuscata Research Articles

Investigating subtle changes in facial expression to assess acute pain in Japanese macaques

Changes in facial expression provide cues for assessing emotional states in mammals and may provide non-verbal signals of pain. This study uses geometric morphometrics (GMM) to explore the facial shape variation in female Japanese macaques who underwent experimental laparotomy. Face image samples were collected from video footage of fourteen macaques before surgery and 1, 3, and 7 days after the procedure. Image samples in the pre-surgical condition were considered pain-free, and facial expressions emerging after surgery were investigated as potential indicators of pain. Landmarks for shape analysis were selected based on the underlying facial musculature and their corresponding facial action units and then annotated in 324 pre-surgical and 750 post-surgical images. The expression of pain is likely to vary between individuals. Tightly closed eyelids or squeezed eyes and lip tension were the most commonly observed facial changes on day 1 after surgery (p < 0.01974). A good overall inter-rater reliability [ICC = 0.99 (95% CI 0.75–1.0)] was observed with the method. The study emphasizes the importance of individualized assessment and provides a better understanding of facial cues to pain for captive macaque care.

Comparative modelling of inspiratory airflow and micron particle deposition patterns in monkey and human nasal airways

Laboratory animals have historically performed a vital function in evaluating health effects of human exposure to ambient particulate matter (PM). Due to the complexity of particle-laden flows and airway interactions that involve multiple species, in-depth knowledge of airflow and particle transport in both the non-human primate surrogates and human airways is still lacking. To advance the understanding in this field, this paper presents a numerical study that investigated the airflow and particle deposition characteristics of inhaled PMs in monkey and human nasal airways. Anatomically accurate macaca fuscata monkey and human nasal cavity models were reconstructed from CT images, micron particles with diameters less than 10 μm were included to conduct in silico exposure studies. Resultant particle deposition patterns were quantified by deposition enhancement factor (DEF) and deposition intensity (DI) along the airways to provide profound understanding of the similarities and differences in particle inhalation exposure characteristics across species. Anatomy comparison showed that the convoluted nasal passage of the monkey airway possessed higher level of complexity in terms of the surface-area-to-volume ratio compared to the two human nasal models, which could lead to higher evaluated nasal exposure to airborne particulate matter. Similar airflow patterns were observed from streamlines and wall shear stress distributions in all three nasal cavities of two species, with bulk air concentrated mainly in the middle and inferior meatuses in the nasal chambers. Despite the evidenced inter-subject deposition variations presented in all considered nasal cavity models, strong and similar micron particle deposition preferences with comparable DEF and DI levels were observed along the floor region of middle and inferior meatuses for both species. The methods and research findings presented in this work represent critical, initial steps towards establishing high-fidelity qualitative and quantitative linkages between the two species that enable more effective laboratory data extrapolations, improve study design, and facilitate validations of in vitro techniques currently being developed as part of international efforts to reduce or replace the use of animals in toxicity assessments for aerosol exposures.

Multiphase processes of seed dispersals via masked palm civets as a non-native species in cool-temperate forests of northern Japan

The disappearance of large seed dispersers such as primates increases the dependence of endozoochorous plants bearing large fruits on frugivorous mesocarnivores for seed dispersal. Ecosystems in northern Japan are typical examples wherein the distribution and abundance of large-sized dispersers (i.e., Macaca fuscata and Ursus thibetanus) have been constrained mainly owing to past anthropogenic disturbances. Moreover, the distribution of several native mesocarnivores has been fragmented, although masked palm civet, Paguma larvata, a non-native frugivorous mesocarnivore, has expanded its distribution over the past quarter-century. Here, we evaluated the roles of this non-native species in defaunated cool-temperate forests by assessing primary and secondary seed dispersal via civets. To assess the primary dispersal process, we identified their possible latrines, where seeds were initially dispersed, by tracking radio-tagged civets. We then compiled an inventory of seeds transported by civets combining the results of the fecal analysis performed in this study and a literature survey for seeds known to be transported by civets. To explore secondary seed dispersals, we first determined the ability of civet feces to attract dung beetles using pitfall traps and then compared this ability of civet feces with that of the feces of raccoon dog, Nyctereutes procyonoides, a native mesocarnivore. Our findings showed that (1) over 90% of the civet latrines confirmed within forested areas with flat terrain, safe sites for germination and establishment of common plant seeds, and carried seeds of 20 plant species; (2) the civet feces were more strongly preferred by dung beetles than raccoon dog feces; and (3) the abundance of large tunneler beetles with superior seed burial ability using the civet feces was 3.7 times as high as that of raccoon dog feces. Thus, these findings suggest that this non-native mesocarnivore could recover functional redundancy by offsetting injured endozoochorous processes.

Time dependence of 137Cs contamination in wild Japanese monkeys after the Fukushima Daiichi nuclear accident

Over the 10 years immediately after the Fukushima Daiichi nuclear accident, we measured the changes in the muscle 137Cs concentration (Bq/kg) of wild Japanese monkeys living in Fukushima City, which is located approximately 70 km from the Fukushima Daiichi Nuclear Power Plant. The muscle137Csconcentration, which was observed at a maximum of 13,500 Bq/kg immediately after the accident, had decreased to several hundred Bq/kg 10 years later. The muscle 137Cs concentration was significantly related to the soil contamination levels (10,000–30,000, 30,000–60,000, 60,000–100,000, and 100,000–300,000 Bq/m2), sex, age class (immature, mature), body weight (> 5000 g, 5000–10,000 g, < 10,000 g), and seasons (the cold period from December to April, the warm period from May to November).The value of muscle 137Cs concentration and the aggregated transfer factor (Tag: calculated by dividing muscle 137Cs concentration [Bq/kg] by soil 137Cs deposition density at the capture site [Bq/m2]) apparently decreased with time for several years. However, post hoc pairwise comparisons showed no difference from 2017 to 2020, and the accumulation of 137Cs in muscle may continue for some time.

The evolution of primate vocal communication: a social route

There is no doubt that different factors determine the evolutionary trajectory of a species' communication abilities. Beyond habitat, social life is likely a selection pressure. The hypothesis positing that living in a complex social system requires complex communication skills has gained ground. However, the measures used classically to tackle this question (i.e. number of call types and group size) fail to capture some of the subtleties of the evolution of communication systems. Integrative approaches comparing closely related species to highlight the possible relationship between the characteristics of their social systems, their ecological niche and associated vocal communication systems are required to further our understanding of this evolutionary puzzle. We first addressed this topic in two sympatric guenons, Diana monkeys and Campbell’s monkeys. Interspecies competition, and the niche specialisations this creates, appeared to be a key evolutionary driver of their repertoires. While most of their vocal units were shared, we found a diversification of alarm calls and socially meaningful vocal combinations, as well as a differential use of inconspicuous (less detectable) call structures. This was linked to differences in group size and degree of exposition to predators. Secondly, we compared the acoustic structures in macaques belonging to four species with contrasting social styles. We found that tolerant (Tonkean and crested) macaques displayed higher levels of vocal diversity (number of vocal units) and flexibility (degree of gradation) than intolerant (Japanese and rhesus) macaques in agonistic and affiliative (but not neutral) contexts. Lastly, because the core of communication is represented not only by what is expressed by an isolated caller, but also by the way vocal interactions are structured, we explored ‘conversational rules’ in apes. We found no relationship between classical social (group size, interaction rates) and vocal (repertoire size, call rates) complexity metrics. However, close call interaction patterns differed in line with the nature of societies. Orang-utan, the most solitary species, preferentially used repeated and isolated calls apparently outside of any vocal interactions. Chimpanzee, the most competitive species displayed a high proportion of overlapping vocalisations. Vocal turn-taking predominated in the most tolerant species (bonobo and gorilla). Even if primate vocal repertoires change slowly over evolutionary time, making them good phylogenetic indicators, socio-ecological niches may induce considerable local divergence at different levels: vocal repertoire composition, acoustic structure and contextual use of calls, and vocal interaction patterns.

Early neurogenic properties of iPSC-derived neurosphere formation in Japanese macaque monkeys

Non-human primates are important models for investigations of neural development and evolution, and the use of Japanese macaque monkeys has especially contributed to the advancement of neuroscience studies. However, these studies are restricted by the number of animals able to be evaluated and the invasiveness of the methodologies. Induced pluripotent stem cells (iPSCs) can provide an alternative strategy for investigating neural development in vitro. We have established direct neurosphere (dNS) formation cultures of primate iPSCs as an in vitro model of early neurodevelopment in primate species. Here, we used dNS formation and neuronal differentiation cultures established from Japanese macaque iPSCs (jm-iPSCs) to investigate the usefulness of these cells as an in vitro model of early neural development. Time-course analyses of developmental potency and gene expression kinetics were performed during dNS formation culture of jm-iPSCs. During a 1-week culture, jm-iPSC-derived dNSs became neurogenic by day 3 and underwent stepwise expression changes of key developmental regulators along early neural development in a similar manner to chimpanzee dNS formation previously reported. Meanwhile, a subset of genes, including CYP26A1 and NPTX1, showed differential expression propensity in Japanese macaque, chimpanzee, and human iPSC-derived dNSs. Spontaneous upregulation of NOTCH signaling-associated genes HES5 and DLL1 was also observed in neuronal differentiation cultures of Japanese macaque but not chimpanzee dNSs, possibly reflecting the earlier neurogenic competence in Japanese macaques. The use of jm-iPSCs provides an alternative approach to neurological studies of primate development. Furthermore, jm-iPSCs can be used to investigate species differences in early neural development that are key to primate evolution.

Process of Japanese macaque group fission at Arashiyama and the influences of maternal kin relations and social relations between adult males and females on it.

In 1986, the Japanese macaques of Arashiyama B group fissioned into Arashiyama E and F groups through the following process. In December 1985, the death of the beta male triggered aggressive interactions among the adult males of B group, leading to a decline in the ranks of two mid-ranked males. Several females started to gather around these two males, formed a stable subgroup (here called the female cluster), and spatially distanced themselves from other group members (main group). Some of these females had mating relations with these two males in previous mating seasons. After the end of the 1985-86 mating season, agonistic interactions occurred frequently between the female cluster and main group. Eventually, two independent groups were established. The females within the 4th degrees of matrilineal consanguinity tended to belong to the same group, but no such tendency occurred in those dyads separated by the 5th or more degrees. After the completion of group fission, mating occurred only a few times between E and F group members. In 1986, when the group fission was in progress, the birth rate of both branch groups declined, and infant mortality increased in E group. After 1987, the birth rate recovered in both branch groups although infant mortality remained high.

Optimizing habitat connectivity among macaque populations in modern Japan

AbstractNationwide depopulation in modern Japan has led to contrasting changes over the last half‐century: shrinking human communities and recovering populations of Japanese macaques (Macaca fuscata). These changes have triggered macaque damage to public livelihoods, often resulting in decision‐making directed toward strictly regulating macaque populations. To optimize conservation interventions required today, we aimed to identify macaque habitats with conservation priorities to enhance population connectivity. To quantify the current population connectivity, we conducted a least‐cost path analysis by assigning an inverse of habitat suitability as resistance. For this, we collected geo‐information on home ranges of 2288 troops, accounting for &gt;70% of the total number of troops in Japan. Moreover, we composed a minimum spanning tree using least‐cost paths to provide optimal population connectivity. Consequently, the modeled resistance showed that, although human‐induced barriers (i.e., flat areas where people frequently reside) and geographical barriers (i.e., alpine regions &gt;1500 m above sea level) had the highest dispersal cost, macaques presented a high plasticity in the occupation of different forest types. The minimum spanning tree, composed of 77 modeled corridors, detected the vulnerability of population connectivity in western Japan and assigned conservation priorities to these isolated populations to preserve the stepping‐stone paths of macaque movement.

Seasonal responses and host uniqueness of gut microbiome of Japanese macaques in lowland Yakushima.

BackgroundChanges in the gut microbial composition is an important response to cope with the seasonal fluctuations in the environment such as food availability. We examined the bacterial gut microbiome of the wild nonhuman primate, Japanese macaque (Macaca fuscata) in Yakushima over 13 months by noninvasive continuous sampling from three identified adult females.ResultsDietary composition varied considerably over the study period and displayed marked shifts with the seasons. Feeding of leaves, fruits, and invertebrates were their main foods for at least one month. Diet had a significant influence on the gut microbiome. We also confirmed significant effect of host uniqueness in the gut microbiome among the three macaques. Leaf-dominated diet shaped unique gut microbiome structures where the macaques had the highest alpha diversity and their gut microbiome was enriched with Spirochaetes and Tenericutes. Diet-related differences in the putative function were detected, such as a differentially abundant urea cycle during the leaf-feeding season.ConclusionBoth diet and host individuality exerted similar amounts of effect on gut microbe community composition. Major bacterial taxa showed a similar response to monthly fluctuations of fruit and invertebrate feeding, which was largely opposite to that of leaf feeding. The main constituents of fruits and invertebrates are both digestible with the enzyme of the host animals, but that of leaves is not available as an energy source without the aid of the fermentation of the gut microbiome.Supplementary InformationThe online version contains supplementary material available at 10.1186/s42523-022-00205-9.

Detailed comparative analysis of environmental microparticle deposition characteristics between human and monkey nasal cavities using a surface mapping technique

Inhaled particulate matter is associated with nasal diseases such as allergic rhinitis, rhinosinusitis and neural disorders. Its health risks on humans are usually evaluated by measurements on monkeys as they share close phylogenetic relationship. However, the reliability of cross-species toxicological extrapolation is in doubt due to physiological and anatomical variations, which greatly undermine the reliability of these expensive human surrogate models. This study numerically investigated in-depth microparticle transport and deposition characteristics on human and monkey (Macaca fuscata) nasal cavities that were reconstructed from CT-images. Deposition characteristics of 1–30μm particles were investigated under resting and active breathing conditions. Similar trends were observed for total deposition efficiencies and a single correlation using Stokes Number was fitted for both species and both breathing conditions, which is convenient for monkey-human extrapolation. Regional deposition patterns were carefully compared using the surface mapping technique. Deposition patterns of low, medium and high inertial particles, classified based on their total deposition efficiencies, were further analyzed in the 3D view and the mapped 2D view, which allows locating particle depositions on specific nasal regions. According to the particle intensity contours and regional deposition profiles, the major differences were observed at the vestibule and the floor of the nasal cavity, where higher deposition intensities of medium and high inertial particles were shown in the monkey case than the human case. Comparisons of airflow streamlines indicated that the cross-species variations of microparticle deposition patterns are mainly contributed by two factors. First, the more oblique directions of monkey nostrils result in a sharper airflow turn in the vestibule region. Second, the monkey's relatively narrower nasal valves lead to higher impaction of medium and high inertial particles on the nasal cavity floor. The methods and findings in this study would contribute to an improved cross-species toxicological extrapolation between human and monkey nasal cavities.

Fission-fusion dynamics in a wild group of Japanese macaques (Macaca fuscata) on Kinkazan Island caused by the repeated separation of an alpha male being followed by females.

The spatiotemporal cohesion of a group is an essential element of primate society. It is thus important to clarify the factors that influence the extent of variation in spatial cohesion and individual membership in a group over time, known as fission-fusion dynamics. During the mating season of 2019, the alpha male (TY) in a wild group of Japanese macaques on Kinkazan Island repeatedly disappeared from the group, and we observed fission-fusion dynamics caused by his movement. The group seemed to have split when TY left the group or its home range, and females who followed him had the most affiliative relationships with TY or were the relatives of those females. Although TY disappeared from the group in the post-mating season, these fission-fusion dynamics only occurred during the mating season probably because females had a more substantial need for protection against aggression from the other males during the mating season. These results indicate that, although rare, fission-fusion dynamics based on affiliative relationships between males and females can occur with the separation of alpha males from the group. More studies in other populations are needed to clarify the influence of group males on the spatial cohesion of groups.

Posture Control Associated with Quadrupedal and Bipedal Gait in Japanese Monkeys (Macaca fuscata)

How the CNS deals with instability of upright posture is the core in the control of bipedal gait. In this review, we summarize our recent findings comparing kinematics and EMG activity during quadrupedal and bipedal gait in Japanese macaques. Trunk/hindlimb muscles showed step cycle-modulated activity, which was more active in bipedal than in quadrupedal gait. For bipedal gait, enhanced activity during longer double support phase was predominantly observed in distal hindlimb muscles. Alternate burst activity in bilateral back muscles cyclically brought back the tilted trunk. In monkeys' quadrupedal gait, hindlimbs formed functional pairs with contralateral forelimbs, unlike in non-primate quadrupeds. These diagonal pairs acted differently on movements of the center of mass (COM). For bipedal gait, the hindlimbs solely carried the COM. Our results suggest that, compared to non-primate quadrupeds, hindlimbs in macaques contribute more critically to weight support and balance control even for quadrupedal gait. Additionally, for more unstable bipedal gait, the monkeys' CNS reinforces such hindlimb roles and actively controls the trunk posture in maintaining dynamic balance, in a manner similar to humans. Studies on Japanese macaques will further our understanding of the neural basis for the control of gait in mammals by bridging non-primate quadrupeds and humans.

Population genetics study of Strongyloides fuelleborni and phylogenetic considerations on primate-infecting species of Strongyloides based on their mitochondrial genome sequences

Strongyloides is a genus of parasitic nematodes of vertebrates comprising approximately 50 documented species, each with various host ranges. Among these, three species (S. stercoralis, S. fuelleborni, and S. cebus) are known to infect primate hosts. S. fuelleborni typically infects non-human primates in the Old World. To complement the existing information on the global genetic structure of this species, we conducted a genotyping study of S. fuelleborni samples collected from rhesus macaques in Myanmar, Japanese macaques in Japan, and some zoo-kept primates. This study identified a novel haplotype group in isolates from the Myanmar rhesus macaques. Subsequently, we obtained the complete or nearly complete mitochondrial genome sequences of S. fuelleborni, S. cebus (Strongyloides of New World monkeys), and S. vituli (Strongyloides of cattle). Phylogenetic analysis based on concatenated mitochondrial protein sequences of various Strongyloides species indicated a close relationship between S. fuelleborni, S. vituli and S. papillosus (Strongyloides in sheep and cattle). S. cebus is quite distantly related to both S. fuelleborni and S. stercoralis, which led to the hypothesis that the three primate Strongyloides species evolved independently as parasites of primates.

Expression of Transcription Factor ZBTB20 in the Adult Primate Neurogenic Niche under Physiological Conditions or after Ischemia.

The Zbtb20 gene encodes for a transcription factor that plays an important role in mammalian cortical development. Recently, its expression was reported in the adult mouse subventricular zone (SVZ), a major neurogenic niche containing neural stem cells throughout life. Here, we analyzed its expression in the adult primate anterior SVZ (SVZa) and rostral migratory stream (RMS) using macaque monkeys (Macaca fuscata). We report that the majority of Ki67+ cells, 71.4% in the SVZa and 85.7% in the RMS, co-label for ZBTB20. Nearly all neuroblasts, identified by their Doublecortin expression, were positive for ZBTB20 in both regions. Nearly all GFAP+ neural stem cells/astrocytes were also positive for ZBTB20. Analysis of images derived from a public database of gene expression in control/ischemic monkey SVZa, showed evidence for ZBTB20 upregulation in postischemic monkey SVZa. Furthermore, the co-localization of ZBTB20 with Doublecortin and Ki67 was increased in the postischemic SVZa. Our results suggest that ZBTB20 expression is evolutionarily conserved in the mammalian neurogenic niche and is reactive to ischemia. This opens the possibility for further functional studies on the role of this transcription factor in neurogenesis in primates.

Mild movement sequence repetition in five primate species and evidence for a taxonomic divide in cognitive mechanisms

When animals forage, they face complex multi-destination routing problems. Traplining behaviour—the repeated use of the same route—can be used to study how spatial memory might evolve to cope with complex routing problems in ecologically distinct taxa. We analyzed experimental data from multi-destination foraging arrays for five species, two cercopithecine monkeys (vervets, Chlorocebus pygerythrus, and Japanese macaques, Macaca fuscata) and three strepsirrhines (fat-tailed dwarf lemurs, Cheirogaleus medius, grey mouse lemurs, Microcebus murinus, and aye-ayes, Daubentonia madagascariensis). These species all developed relatively efficient route formations within the arrays but appeared to rely on variable cognitive mechanisms. We found a strong reliance on heuristics in cercopithecoid species, with initial routes that began near optimal and did not improve with experience. In strepsirrhines, we found greater support for reinforcement learning of location-based decisions, such that routes improved with experience. Further, we found evidence of repeated sequences of site visitation in all species, supporting previous suggestions that primates form traplines. However, the recursive use of routes was weak, differing from the strategies seen in well-known traplining animals. Differences between strepsirrhine and cercopithecine strategies may be the result of either ecological or phylogenetic trends, and we discuss future possibilities for disentangling the two.

The effect of different body positions on the cardiothoracic ratios obtained by chest radiography in Japanese macaques (Macaca fuscata) and rhesus macaques (Macaca mulatta).

Although some studies have reported cardiac diseases in macaques, an adequate screening method for cardiac enlargement has not yet been established. This study aimed to evaluate the positioning of macaques for radiographs and establish reference intervals for the cardiothoracic ratio (CTR). We developed a device for chest radiography in the sitting position and performed chest radiography in 50 Japanese and 48 rhesus macaques to evaluate the CTR and chest cavity size. In Japanese and rhesus macaques, the thorax height was significantly larger, the heart width was significantly smaller, and the mean CTR was significantly smaller in the sitting position than in the prone position. The reference intervals for CTR in the sitting position were 51.6 ± 4.6% and 52.2 ± 5.1% in Japanese and rhesus macaques, respectively. Thoracic radiographic images obtained in a sitting position resulted in a smaller CTR and a larger thorax height, which could be useful for detecting pulmonary and cardiac abnormalities.

Monkey Prefrontal Single-Unit Activity Reflecting Category-Based Logical Thinking Process and Its Neural Network Model.

Category-based thinking is a fundamental form of logical thinking. Here, we aimed to investigate its neural process at the local circuit level in the prefrontal cortex (PFC). We recorded single-unit PFC activity while male monkeys (Macaca fuscata) performed a task in which the category and rule were prerequisites of logical thinking and the outcome contingency was its consequence. Different groups of neurons coded a single type of information discretely or multiple types in a transitional form. Results of time-by-time analysis of neuronal activity suggest an information flow from category-coding and rule-coding neurons to transitional intermediate neurons, and then to contingency-coding neurons. Category-coding, rule-coding, and contingency-coding neurons showed stable coding of information, whereas intermediate neurons showed dynamic coding, as if it integrated category and rule to derive contingency. A similar process was confirmed by using a spiking neural network model that consisted of subnetworks coding category and rule on the input layer and those coding contingency on the output layer, with a subnetwork for integration in the intermediate layer. These results suggest that category-based logical thinking is realized in the PFC by separated neural populations organized for working in a feedforward manner.SIGNIFICANCE STATEMENT To elucidate the neural process for logical thinking, we combined an in-depth analysis of single-unit activity data with a biologically plausible computational model. Results of time-by-time analysis of prefrontal neuronal activity suggest an information flow from category-coding and rule-coding neurons to transitional intermediate neurons, and then to contingency-coding neurons. Category-coding, rule-coding, and contingency-coding neurons showed stable coding, whereas intermediate neurons showed dynamic coding, as if they integrated category and rule to derive contingency. A spiking neural network model reproduced similar temporal changes of information as the recorded neuronal data. Our results suggest that the prefrontal cortex (PFC) is critically involved in category-based thought process, and this process may be produced by separated neural populations organized for working in a feedforward manner.

Maternal Western-style diet reduces social engagement and increases idiosyncratic behavior in Japanese macaque offspring

Recent evidence in humans and animals indicates an association between maternal obesity and offspring behavioral outcomes. In humans, increased maternal body mass index has been linked to an increased risk of children receiving a diagnosis of early-emerging neurodevelopmental disorders such as Attention Deficit/Hyperactivity Disorder (ADHD) and/or Autism Spectrum Disorder (ASD). However, a limited number of preclinical studies have examined associations between maternal Western-Style Diet (mWSD) exposure and offspring social behavior. To our knowledge, this is the first study to investigate relationships between mWSD exposure and social behavior in non-human primates. Since aberrant social behavior is a diagnostic criterion for several neurodevelopmental disorders, the current study focuses on examining the influence of maternal nutrition and metabolic state on offspring social behavior in Japanese macaques (Macaca fuscata). We found that mWSD offspring initiated less affiliative social behaviors as well as proximity to a peer. Using path analysis, we found that the association between mWSD consumption and reduced offspring social engagement was statistically mediated by increased maternal interleukin (IL)-12 during the third trimester of pregnancy. Additionally, mWSD offspring displayed increased idiosyncratic behavior, which was related to alterations in maternal adiposity and leptin in the third trimester. Together, these results suggest that NHP offspring exposed to mWSD exhibit behavioral phenotypes similar to what is described in some early-emerging neurodevelopmental disorders. These results provide evidence that mWSD exposure during gestation may be linked to increased risk of neurodevelopmental disorders and provides targets for prevention and intervention efforts.

My path to primatology: some stories from the field.

In this paper, I summarize the major facets of my 50-year career as a primatologist. I briefly describe the aspects of my upbringing and early education that led me to the study of primate behavior, first in captive settings and, later, in the wild. My research on the Arashiyama West Japanese macaques and my interactions with Japanese primatologists was a formative stage in my career, and I present the background of this international project and how it led to my growing focus on female life history studies. After a couple of failed attempts to establish a long-term study of primates in their native habitats, I began the Santa Rosa Primate Project in Costa Rica in 1983, which focuses mainly on white-faced capuchins, and to some extent on howlers and spider monkeys. The Santa Rosa project has expanded over the past four decades and continues to this day, with the participation of a large team of colleagues, local field assistants and students. I present some of the major findings of our Santa Rosa monkey research in the areas of female reproduction, sexual conflict and conservation of primates in a regenerating tropical dry forest. I also briefly describe how and why I came to develop a sideline of research on gender and science.

Chemical cues of identity and reproductive status in Japanese macaques.

Olfactory communication plays an important role in the regulation of socio-sexual interactions in mammals. There is growing evidence that both human and nonhuman primates rely on odors to inform their mating decisions. Nevertheless, studies of primate chemical ecology remain scarce due to the difficulty of obtaining and analyzing samples. We analyzed 67 urine samples from five captive female Japanese macaques (Macaca fuscata) and 30 vaginal swabs from three of these females using gas chromatography-mass spectrometry and examined the relationship between odor (compounds identified, richness, intensity, and diversity) and female identity as well as cycle phase. We found a total of 36 urine compounds of which we identified 31, and 68 vaginal compounds of which we identified 37. Our results suggest that urine and vaginal odor varied more between individuals than within cycle phases. However, we found that within a female cycle, urine samples from similar phases may cluster more than samples from different phases. Our results suggest that female odor may encode information about identity (vaginal and urine odor) and reproductive status (urine odor). The question of how conspecifics use female urine and vaginal odor remains open and could be tested using bioassays. Our results and their interpretation are constrained by our limited sample size and our study design. Nonetheless, our study provides insight into the potential signaling role of female odor in sexual communication in Japanese macaques and contributes to our understanding of how odors may influence mating strategies in primates.