Behavior In Japanese Macaques Research Articles

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.

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.

Do dominant monkeys gain more warmth? Number of physical contacts and spatial positions in huddles for male Japanese macaques in relation to dominance rank

Animals show various forms of behavioral thermoregulation to minimize cold stress. Given that higher dominance rank is often associated with increased fitness in group-living animals, higher-ranking individuals may also benefit from better access to thermally optimal spatial positions within huddles. This study examined the association between dominance rank and the potential thermoregulatory benefits of huddling behavior in Japanese macaques (Macaca fuscata) inhabiting Shodoshima Island, which form exceptionally large huddles. I photographed monkey huddles, and analyzed the number of individuals that males were in contact with and males’ spatial positons in huddles. Higher-ranking males were significantly more likely to be in contact with larger numbers of individuals in huddles. Higher-ranking males occupied non-peripheral positions in huddles more often than lower-ranking males, which put them in contact with larger numbers of individuals. These results suggest that high dominance rank may confer potential thermal advantages on male Japanese macaques. The mechanism for this is likely that the highest-ranking male often intrude in already-formed huddles, although such behaviors of males were not quantitatively assessed. This study contributes to a better understanding of the mechanisms of cold adaptation in relation to dominance rank in group-living animals.

Report on a web-based questionnaire on infrequently observed behaviors in Japanese macaques, referring to their video footage, with special reference to cultural differences among populations

Report on a web-based questionnaire on infrequently observed behaviors in Japanese macaques, referring to their video footage, with special reference to cultural differences among populations

Variation in Adult Male-Juvenile Affiliative Behavior in Japanese Macaques (Macaca fuscata)

Adult males of some primate species are known to positively interact with juveniles. In cases where paternal certainty is high, these behaviors have been largely attributed to the paternal investment hypothesis. Males have also been observed to interact with nonkin juveniles, which has often been explained in terms of mating effort. Here, we examined variation in adult male-juvenile affiliation in semi-free ranging Japanese macaques (Macaca fuscata) at the Oregon National Primate Research Center against possible influencing factors such as age, dominance rank, and female affiliation, and we also tested for fitness benefits. We conducted 154 h of focal observations of 14 adult males from June to September 2018. Males differed significantly in their rate of juvenile-directed affiliation, but not in their fitness in terms of number of offspring. There was a significant positive correlation between rank and age in the group, indicating that, in this group, rank does not conform to the classic inverted-U pattern observed elsewhere in this species. Although there was a significant positive correlation between rank and juvenile-directed affiliation, the highest-ranking male had few offspring and exhibited little juvenile-directed affiliation. These results suggest little to no preliminary support for either the paternal investment or mating effort hypotheses as explanations for juvenile-directed affiliation. This study suggests that there are multiple behavioral strategies for older males that may influence reproductive success.

Is female-male mounting functional? An analysis of the temporal patterns of sexual behaviors in Japanese macaques

In certain populations of Japanese macaques, adult females mount adult males in the context of heterosexual consortships (i.e., temporary but exclusive sexual associations between a male and a female). Previous research suggested that, in this primate species, female-male mounting (FMM) may be a behavioral adaptation. This functional hypothesis holds that FMM is a (special) courtship behaviour, or a (super) sexual solicitation, that serves the function of focusing the male's attention, preventing him from moving away, and expediting male-female mounting, in the context of high female competition for male mates. In this study, we aimed to test some of the proposed functional features of FMM in Japanese macaques by comparing the temporal structure of mating behavioral sequences, including various well-known sexual solicitations, exhibited during heterosexual consortships with and without FMM. To identify and compare recurring series of behavioral events within and across sequences, we used a temporal analysis known as “T-pattern detection and analysis”. Our results (partly) supported the “FMM as a (super) sexual solicitation” hypotheses, and supported the “FMM as a sexual adaptation” hypothesis. The utilization of TPA allows for the detection of hidden features of primates’ behaviors otherwise undetectable by using conventional quantitative approaches, such as the calculation of frequencies or durations of isolated behavioral components, disjointed from the comprehensive behavioral architecture. This study fits into the scheme of a broader investigation of the functionality of non-conceptive mounting patterns observed in Japanese macaques and a reconstruction of their evolutionary history.

Maternal Interleukin-6 Is Associated With Macaque Offspring Amygdala Development and Behavior.

Human and animal cross-sectional studies have shown that maternal levels of the inflammatory cytokine interleukin-6 (IL-6) may compromise brain phenotypes assessed at single time points. However, how maternal IL-6 associates with the trajectory of brain development remains unclear. We investigated whether maternal IL-6 levels during pregnancy relate to offspring amygdala volume development and anxiety-like behavior in Japanese macaques. Magnetic resonance imaging (MRI) was administered to 39 Japanese macaque offspring (Female: 18), providing at least one or more time points at 4, 11, 21, and 36 months of age with a behavioral assessment at 11 months of age. Increased maternal third trimester plasma IL-6 levels were associated with offspring's smaller left amygdala volume at 4 months, but with more rapid amygdala growth from 4 to 36 months. Maternal IL-6 predicted offspring anxiety-like behavior at 11 months, which was mediated by reduced amygdala volumes in the model's intercept (i.e., 4 months). The results increase our understanding of the role of maternal inflammation in the development of neurobehavioral disorders by detailing the associations of a commonly examined inflammatory indicator, IL-6, on amygdala volume growth over time, and anxiety-like behavior.

Testing for Links Between Female Urine Odor and Male Sexual Behaviors in Japanese Macaques (Macaca fuscata)

Urine is involved in sexual communication in New World monkeys and lemurs, but most studies of the role of olfaction in sexual communication in Old World monkeys have focused on vaginal secretions rather than urine. We investigated whether female urine promotes male sexual behaviors (approaches and inspections of genital area) in Japanese macaques (Macaca fuscata). We used a sequential presentation paradigm in behavioral experiments, presenting unfamiliar female urine and control cotton swabs to males living in a social group with cycling females. We tested whether males (N = 3) showed more processing behaviors (licking, sniffing, tasting) toward female urine (22 stimuli per male from prefertile, fertile, and postfertile phases, based on urinary estrone and progesterone conjugate profiles) than control odor (8 stimuli per male). We then compared male sexual behaviors toward resident females pre- and post-exposure to stimuli and in relation to the females’ reproductive status (perifertile, nonfertile, and pregnancy periods, based on fecal estrone and progesterone conjugate profiles). We found that males showed significantly more processing behaviors toward urine stimuli than to controls but that male behavior did not vary across urine samples from prefertile, fertile, and postfertile phases. Exposure to unfamiliar female urine stimuli did not modulate male approaches to and inspections of resident females at any stage of the female reproductive cycle. Although our study is limited by its small sample size, the results suggest that female urine contains compounds that males detect, but we found no evidence that female urine is related to male sexual behaviors.

Effect of Female-Biased Sex Ratios on Female Homosexual Behavior in Japanese Macaques: Evidence for the "Bisexual Preference Hypothesis".

We aimed to explain the frequent and prevalent female homosexual behavior in the context of female-biased operational sex ratios (OSR) and qualified sex ratios (Q) in a free-ranging group of Japanese macaques (Macaca fuscata) living at Arashiyama-Kyoto, Japan. Our data included the average availability of sexually mature males during females' putative fertile period (OSR), the ratio of sexually mature males to sexually mature females (Q), as well as heterosexual and female homosexual solicitations and consortships collected during 13 mating seasons from 136 females. Our results did not support the "heterosexual deprivation hypothesis," which holds that female homosexual behavior is attributable to a shortage of male mates. Likewise, our results did not support the "lack of opposite-sex sexual competitor hypothesis," which holds that females have more access to female mates when male sexual rivals are scarce. Of the 11 predictions tested, only one yielded statistically significant results: we found that higher ratios of availability of preferred female partners to preferred male partners were associated with female homosexual consortships rather than female heterosexual consortships. This result supported the "bisexual preference hypothesis," which holds that female homosexual behavior is attributable to female preference for certain female mates relative to certain male mates. We conclude that when a female targets another female as a mate, it is an active choice for a female sexual partner over available male alternatives, rather than a by-default situation that occurs because males are not available as sexual partners, or because females are better able to access female sexual partners due to a scarcity of male sexual competitors.

Influence of sexual competition and social context on homosexual behavior in adolescent female Japanese macaques.

We explored the role that sexual and social partners play in the expression of female homosexual behavior among adolescent female Japanese macaques at Arashiyama, Japan. Our data fully or partially supported all the predictions related to four non-mutually exclusive hypotheses, namely the "adult male disinterest in adolescent females" hypothesis, the "numerous homosexual adult females" hypothesis, the "safer homosexual interactions" hypothesis and the "same-sex sexual interactions" hypothesis. Our results show that both sexual context (e.g., lack of adolescent female attractivity toward adult males, presence of motivated same-sex sexual partners), and social context (e.g., risk of aggression) help explain the high frequency and prevalence of homosexual behavior in adolescent females in the Arashiyama group of Japanese macaques. As with adult females, whose homosexual consortships do not reflect generalized patterns of social affiliation or kinship, we found that adolescent females' same-sex sexual partners were neither kin, nor were they non-kin individuals with whom adolescent females were closely affiliated outside of a consortship context. Our study furthers the growing database of female homosexual behavior in Japanese macaques and provides additional evidence that homosexual behavior as expressed by adolescent female Japanese macaques is, like heterosexual behavior, sexual in nature. We discuss the relevance of our findings to a broader comparative approach that may shed light upon the development and evolution of human homosexuality.

Stone handling behavior in rhesus macaques (Macaca mulatta), a behavioral propensity for solitary object play shared with Japanese macaques

Stone handling (SH) behavior was systematically studied in a captive troop of rhesus macaques housed at the Primate Research Institute of Kyoto University, and compared with the results of long-term studies of this behavior in Japanese macaques, to evaluate the similarities of SH behavior in these two closely related species. Similar to Japanese macaques, rhesus macaques showed age-related differences in SH. Young animals were more active and displayed more SH patterns and bouts than did adults. Furthermore, the young displayed SH at a higher frequency and their bouts were of a shorter duration, compared to adults. Young adults were more active and displayed more patterns than did older adults. On the other hand, older adults were more conservative and displayed fewer patterns, and engaged in them for longer durations. All individuals displayed SH more frequently in relaxed environmental and social conditions. While lacking an apparent immediate adaptive value, practice of the behavior has been proposed to have long-term functional value for neural and cognitive development in the young and for the maintenance or repair of neuro-pathways in aging macaques that habitually perform the behavior. The results presented here are consistent with what we know about Japanese macaque SH. Given the uniformity of SH behavioral parameters and these two macaque species' close phylogenetic relatedness, we propose that a similar functional and adaptive value for SH can be inferred for rhesus macaques.

Non-lactating versus lactating females: a comparison of sex steroids, sexual coloration, and sexual behavior in Japanese macaques

Female Japanese macaques are seasonal breeders distinguished by their red-colored hindquarters, face, and nipple skin areas. Intensity of coloration seems to be associated with sexual attractiveness, behavior, and fluctuating sex steroids. Our aim was to investigate whether the color intensity of these regions differed between lactating (LA) and non-lactating (NLA) females during sexually inactive (SI) and active (SA) phases. Coloration scores of 19 adult females were classified using color tables. Estrogen and progesterone metabolites were determined in fecal samples. Weekly comparison between both groups revealed significantly increased coloration of the hindquarters area from week 13 (SI) until the end of the observation period, and for the nipple skin throughout the SI and SA periods. Face coloration differed marginally. Hormonally, NLA females showed significantly increased excretion rates of sex steroids at the end of the SI phase and throughout the whole SA period. Logistic regression analyses between elevated fecal steroids and nipple coloration disclosed a significant relationship for NLA females during the SI period. This connection persisted and included hindquarter coloration during the SA period. NLA females showed increased intromission with ejaculation, but no difference was found for intromission without ejaculation. In conclusion, results demonstrate increased endocrine excretion rates for NLA females during the whole observation period, paralleled by an enhanced, fertility-signaling sexual attractiveness.

Indirect social influence in the maintenance of the stone-handling tradition in Japanese macaques, Macaca fuscata

Comparative and longitudinal studies have shown that stone-handling (SH) behaviour, defined as the noninstrumental manipulation of stones by performing various behavioural patterns, is socially transmitted across generations as a cultural behaviour in Japanese macaques. We investigated experimentally how stimulus/local enhancement, a form of indirect social influence through the physical traces typically left in the environment by previous stone handlers, might trigger SH behaviour at the individual level, and thus could contribute to the maintenance of the SH tradition at the group level. Through the semicontrolled conditions of field experiments, conducted in the free-ranging provisioned Arashiyama E troop, in which the SH tradition has been well established for nearly three decades, our results supported the stimulus/local enhancement hypothesis. Most group members preferentially directed their SH behaviour towards typical physical traces of SH activity (piles of stones) over randomly scattered stones. Encountering SH artefacts enhanced the use of these particular stones for performing SH in that particular part of the environment. The common occurrence of such ‘play stations’ may favour the frequent reuse of the same stones over time and explain the transport of stones between and around SH artefacts. We provided evidence for the role of indirect social inputs on the long-term persistence of the SH tradition in Japanese macaques, through SH by-products, the stimulating effect of which can be delayed in time and separate in space from others. We discuss our findings from the perspective of socially mediated behaviours, conformity-enforcing responses and niche construction.

The Biogeography and Evolution of Female Homosexual Behavior in Japanese Macaques

In certain Japanese macaque (Macaca fuscata) populations, females routinely engage in same-sex courtship, mounting, and consortship activity. Drawing on behavioral, biogeographic, and genetic research, we suggest that female homosexual behavior may be associated with genetically distinct free-ranging populations of Japanese macaques. In addition, we briefly discuss the implications of this research for the evolution of female homosexual behavior in this species.

Courtship behaviour in Japanese macaques during heterosexual and homosexual consortships

Female Japanese macaques (Macaca fuscata) in the Arashiyama population near Kyoto, Japan, are unusual, in that they exhibit what many would consider to be male-typical sexual characteristics. Specifically, they mount other females within the context of temporary, but exclusive, sexual relationships (i.e., homosexual consortships) and they sometimes exhibit a preference for female sexual partners, even when given the choice of a sexually motivated male alternative. In this study, we examined whether female Japanese macaques also exhibited male-typical patterns of courtship behaviour during homosexual consortships. Data were collected on courtship behaviour during heterosexual and homosexual consortships in free-ranging Japanese macaques from the Arashiyama (Japan) population. We analyzed the occurrence of 12 different courtship behaviours during 3374 heterosexual inter-mount intervals and 1412 homosexual inter-mount intervals. Sex differences between heterosexually consorting males and females existed for only two of the 12 courtship behaviours we investigated: inclined-back presentations and sexual vocalizations. Dominant and subordinate homosexually consorting females were sex-typical in their expression of inclined-back presentations and sexual vocalizations. Consequently, facultative same-sex sexual partner preference, mounting and consortships do not co-occur with male-typical patterns of courtship behaviour in female Japanese macaques.

Comparative and longitudinal approaches in cultural primatology: the case of stone handling behavior in Japanese macaques

Comparative and longitudinal approaches in cultural primatology: the case of stone handling behavior in Japanese macaques

Pre- and Postconflict Interactions Between Female Japanese Macaques During Homosexual Consortships

In this paper, I examine whether homosexual behavior in female Japanese macaques functions to reconcile conflicts following the outbreak of aggression. Contrary to the predictions of the reconciliation hypothesis, homosexual interactions between female Japanese macaques did not peak during postconflict periods, as compared to matched control periods preceding the conflicts. In fact, aggressive interactions appeared to inhibit, rather than facilitate, the expression of homosexual behavior among subordinate consort partners. Alternative proximate and ultimate explanations for female homosexual behavior in Japanese macaques are presented.

Effects of maternal style on infant behavior in Japanese macaques (Macaca fuscata).

We assessed the association of maternal style and infant behavior of group-living Japanese macaques during the first year of infant development. We tested the hypothesis that different mothering styles were correlated with the behavioral repertoire of infants at three different developmental stages. We expected that infants of rejecting mothers would show a higher level of enterprise and that infants of protective mothers would be less interested in the external environment. We found evidence that maternal style affects infant behavior during the early developmental phase, but this influence becomes smaller as the infant grows older and approaches complete independence. Maternal protectiveness appears to have long-lasting effects on infant exploration as infants of protective mothers tended to be less attracted by the external environment. On the other hand, mater- nal rejection appears to have long-lasting effects on infant interaction with other group members as more rejected infants tended to initiate a significantly higher number of contacts with other juveniles and adults. These results suggest that both maternal rejection and maternal protectiveness play an important role in the independence of the offspring, in opposite directions. That is, rejection promotes independence whereas protectiveness delays it.

Long-Term Trends in Matrilineal Inbreeding Among the Japanese Macaques of Arashiyama B Troop

In a long-term study of sexual behavior in Japanese macaques, we found that matrilineal inbreeding accounted for 2.9% of the copulations recorded for the Arashiyama B troop during 7 mating seasons between 1968 and 1984. Of the 906 copulatory dyads, 46 (5.1%) occurred among kin. Close matrilineal kin dyads (r = 1/2−1/8, 1.1% of the total of copulatory dyads) strongly avoided matrilineal inbreeding, but for remote kin dyads (r > 1/8, 4.0% of the total) the tendency was weaker in some years. Among the possible determinants of matrilineal inbreeding, we found that it tended to occur among younger and lower-ranking males as an effect of troop demographic changes. There is no significant association between female rank and matrilineal inbreeding. Our results are consistent with the hypothesis that different degrees of kin relatedness are discriminated by individuals with respect to mate choice.

Sexual partner preference in female Japanese macaques.

Whether animals ever exhibit a preference for same-sex sexual partners is a subject of debate. Japanese macaques represent excellent models for examining issues related to sexual preference in animals because females, in certain populations, routinely engage in both heterosexual and homosexual behavior over the course of their life spans. Multiple lines of evidence indicate that female homosexual behavior in Japanese macaques is a sexual behavior, not a sociosexual one. Additional evidence indicates that female Japanese macaques do not engage in homosexual behavior simply because acceptable male mates are unavailable or unmotivated to copulate. Patterns of sexual partner choice by female Japanese macaques that are the focus of intersexual competition indicate that females of this species choose same-sex sexual partners even when they are simultaneously presented with a motivated, opposite-sex alternative. Thus, in some populations of Japanese macaques, females prefer certain same-sex sexual partners relative to certain male mates, and vice versa. Taken together, this evidence suggests that female Japanese macaques are best characterized as bisexual in orientation, not preferentially homosexual or preferentially heterosexual.