Post-conflict Behaviour in Long-tailed Macaques (Macaca fascicularis)

After being the victim of an agonistic conflict, long-tailed macaques increased the rate of tension-related activities such as scratching, body-shake and selfgrooming. This increase indicates that they experienced physiological changes preparing them to cope with the uncertainty of the post-conflict situation. Indeed, victims of agonistic conflict experienced a higher risk of renewed attacks. However, victims were also involved in social interactions characteristic of post-conflict situations, namely reconciliation and redirection. These two post-conflict social events reduced the rate of scratching, body-shake and selfgrooming. This suggests a faster termination of the stress response. Indeed, the two social events also decreased the likelihood of renewed attacks, one of the causes of the state of uncertainty. Reconciliation is more effective than redirection in this process probably because the restoration of the relationship with the former aggressor allows the victim to resume control of the situation.     

Hiding Behaviour of Long-tailed Macaques (Macaca fascicularis): II. Use of Hiding Places during Aggressive Interactions

In an observational study on captive long-tailed macaques ( Macaca fascicularis ), the ability to hide was investigated in the social context of aggression. The use of five different types of hiding place during highly aggressive interactions was recorded and the choices of six different rank-sex classes were compared using an index of attractiveness of the different types of hiding place during highly aggressive interactions. There was no significant difference between the rank-sex classes in selection of the hiding places that could be connected with visibility: no specific location or type was preferred, either by the group as a whole or by any specific rank-sex class. Thus long-tailed macaques do not seem to hide shortly after aggressive interactions.     

Interannual variability in fruit abundance and the reproductive seasonality in Sumatran Long-tailed macaques (Macaca fascicularis)

In an environment with a seasonal food supply, most primate species show birth peaks which precede the peak food period by some two to five months. Sumatran Long-tailed macaques (Macaca fascicularis), however, showed birth peaks during or after the fruit peak. Years of high birth rates and early birth peaks alternated with years of low birth rates and late peaks. The timing of births was strongly influenced by a female's condition, which depends on food supply and her previous reproductive history. Pregnant females were more active than other females, whereas females with young infants were less active.
The unusual timing of births is ascribed to the unpredictability of the height of the annual fruit peak. This hypothesis is supported by the reproductive patterns of other South-east Asian primates and by a model comparing the two types of reproductive timing. Further differences between the two strategies of reproductive timing are predicted.     

Representation of Faces in Longtailed Macaques (Macaca fascicularis)

The experiments described in this study were intended to increase our knowledge about social cognition in primates. Longtailed macaques (Macaca fascicularis) had to discriminate facial drawings of different emotional expressions. A new experimental approach was used. During the experimental sessions social interactions within the group were permitted, but the learning behaviour of individual monkeys was analysed. The procedure consisted of a simultaneous discrimination between four visual patterns under continuous reinforcement. It has implications not only for simple tasks of stimulus discrimination but also for complex problems of internal representations and visual communication. The monkeys learned quickly to discriminate faces of different emotional expressions. This discrimination ability was completely invariant with variations of colour, brightness, size, and rotation. Rotated and inverted faces were recognized perfectly. A preference test for particular features resulted in a graded estimation of particular facial components. Most important for face recognition was the outline, followed by the eye region and the mouth. An asymmetry in recognition of the left and right halves of the face was found. Further tests involving jumbled faces indicated that not only the presence of distinct facial cues but the specific relation of facial features is essential in recognizing faces. The experiment generally confirms that causal mechanisms of social cognition in non-human primates can be studied experimentally. The behavioural results are highly consistent with findings from neurophysiology and research with human subjects.     

Hiding Behaviour of Longtailed Macaques (Macaca fascicularis). I. Theoretical Background and Data on Mating

During an observational study of captive longtailed macaques (Macaca fascicularis), the ability to hide was analysed within the social context of mating. Low- and middle-ranking males and their female partners chose places for mating where they were partly or entirely concealed more often than easily visible places. These places were not the preferred places of either sex in general, although it was also observed that lower-ranking animals of both sexes lead a more inconspicuous life than high-ranking animals. The probable mechanisms of this phenomenon are discussed: trial-and-error learning or a simple rule of thumb seem to be the appropriate explanations since the choice between different structures of hiding places is not as sharply defined as would be expected if ‘perspective taking’ were the mechanism.     

Experimental Infection of Cynomolgus Macaques (Macaca fascicularis) with Aerosolized Monkeypox Virus

Monkeypox virus (MPXV) infection in humans results in clinical symptoms very similar to ordinary smallpox. Aerosol is a route of secondary transmission for monkeypox, and a primary route of smallpox transmission in humans. Therefore, an animal model for aerosol exposure to MPXV is needed to test medical countermeasures. To characterize the pathogenesis in cynomolgus macaques (Macaca fascicularis), groups of macaques were exposed to four different doses of aerosolized MPXV. Blood was collected the day before, and every other day after exposure and assessed for complete blood count (CBC), clinical chemistry analysis, and quantitative PCR. Macaques showed mild anorexia, depression, and fever on day 6 post-exposure. Lymphadenopathy, which differentiates monkeypox from smallpox, was observed in exposed macaques around day 6 post-exposure. CBC and clinical chemistries showed abnormalities similar to human monkeypox cases. Whole blood and throat swab viral loads peaked around day 10, and in survivors, gradually decreased until day 28 post-exposure. Survival was not dose dependent. As such, doses of 4×10⁴ PFU, 1×10⁵ PFU, or 1×10⁶ PFU resulted in lethality for 70% of the animals, whereas a dose of 4×10⁵ PFU resulted in 85% lethality. Overall, cynomolgus macaques exposed to aerosolized MPXV develop a clinical disease that resembles that of human monkeypox. These findings provide a strong foundation for the use of aerosolized MPXV exposure of cynomolgus macaques as an animal model to test medical countermeasures against orthopoxviruses.     

Experimental infection of Cynomolgus Macaques (Macaca fascicularis) with human varicella-zoster virus

Varicella-zoster virus (VZV) is a member of the alphaherpesvirus family and the causative agent of chickenpox and shingles. To determine the utility of cynomolgus macaques (Macaca fascicularis) as a nonhuman primate model to evaluate VZV-based simian immunodeficiency virus/human immunodeficiency virus (SIV/HIV) vaccines, we experimentally inoculated 10 animals with the parental Oka (Oka-P) strain of VZV derived from MeWo or Telo-RF cells. VZV DNA could be detected in the lungs as late as 4 days postinfection, with replicating virus detected by shell vial culture assay in one case. Infection did not result in any overt clinical symptoms but was characterized by humoral and cell-mediated immunity in a time frame and at a magnitude similar to those observed following VZV vaccination in humans. The cell line source of VZV inoculum influenced both the magnitude and polyfunctionality of cell-mediated immunity. Animals mounted a vigorous anamnestic antibody response following a second inoculation 12 weeks later. Inoculations resulted in transient increases in CD4(+) T-cell activation and proliferation, as well as a sustained increase in CD4(+) T cells coexpressing CCR5 and α4β7 integrin. In contrast to previous failed attempts to successfully utilize attenuated VZV-Oka as an SIV vaccine vector in rhesus macaques due to suboptimal infectivity and cellular immunogenicity, the ability to infect cynomolgus macaques with Oka-P VZV should provide a valuable tool for evaluating VZV-vectored SIV/HIV vaccines.     

Pulmonary embolization of fat and bone marrow in cynomolgus Macaques (Macaca fascicularis)

Fat embolization (FE), the introduction of bone marrow elements into circulation, is a known complication of bone fractures. Although FE has been described in other animal models, this study represents the first reported cases of FE and bone marrow embolism in nonhuman primates. Histopathologic findings from cynomolgus macaques (Macaca fascicularis) indicated that in all 5 cases, fat and bone marrow embolization occurred subsequent to multiple bone marrow biopsies. In the most severe case, extensive embolization was associated pulmonary damage consistent with acute respiratory distress syndrome. Fat embolism syndrome (FES) is an infrequent clinical outcome of FE and is triggered by systemic biochemical and mechanical responses to fat in circulation. Although clinical criteria diagnostic of FES were not investigated at the time of death, this severe case may represent the fulminant form of FES, which occurs within 12 h after trauma. Bone marrow biopsy as an etiology of FES has been reported only once in humans. In addition, the association of embolization with bone marrow biopsies suggests that nonhuman primates may be a useful animal model of FE. FE and FES represent important research confounders and FES should be considered as a differential diagnosis for clinical complications subsequent to skeletal trauma.     

Effects of MDMA Injections on the Behavior of Socially-Housed Long-Tailed Macaques (Macaca fascicularis)

3,4-methylenedioxy-N-methyl amphetamine (MDMA) is one of the few known molecules to increase human and rodent prosocial behaviors. However, this effect has never been assessed on the social behavior of non-human primates. In our study, we subcutaneously injected three different doses of MDMA (1.0, 1.5 or 2.0mg/kg) to a group of three, socially housed, young male long-tailed macaques. More than 200 hours of behavioral data were recorded, during 68 behavioral sessions, by an automatic color-based video device that tracked the 3D positions of each animal and of a toy. This data was then categorized into 5 exclusive behaviors (resting, locomotion, foraging, social contact and object play). In addition, received and given social grooming was manually scored. Results show several significant dose-dependent behavioral effects. At 1.5mg/kg only, MDMA induces a significant increase in social grooming behavior, thus confirming the prosocial effect of MDMA in macaques. Additionally, at 1.5 and 2.0 mg/kg MDMA injection substantially decreases foraging behavior, which is consistent with the known anorexigenic effect of this compound. Furthermore, at 2.0 mg/kg MDMA injection induces an increase in locomotor behavior, which is also in accordance with its known stimulant property. Interestingly, MDMA injected at 1.0mg/kg increases the rate of object play, which might be interpreted as a decrease of the inhibition to manipulate a unique object in presence of others, or, as an increase of the intrinsic motivation to manipulate this object. Together, our results support the effectiveness of MDMA to study the complex neurobiology of primates’ social behaviors.     

Compete to Play: Trade-Off with Social Contact in Long-Tailed Macaques (Macaca fascicularis)

Many animal species engage in various forms of solitary object play, but this activity seems to be of particular importance in primates. If playing objects constitute a valuable resource, and access to such objects is limited, a competitive context may arise. We inserted a unique toy within a mini-colony of long-tailed macaque (Macaca fascicularis) and compared their behaviors to sessions without playing object. An automatic color-based 3D video device was used to track the positions of each animal and the toy, and this data was categorized into 5 exclusive behaviors (resting, locomotion, foraging, social contact and object play). As expected, the delay to first access to the object reflected the hierarchy of the colony, indicating that a competition took place to own this unique resource of entertainment. In addition, we found that the amount of object play was not correlated with social or foraging behavior, suggesting independent motivational mechanisms. Conversely, object playing time was negatively correlated with idling time, thus indicating its relation to pastime activities. Interestingly, the amount of social contacts in the group was significantly reduced by the heightened competitive context, suggesting that competitors are more likely to be perceived as potential threat requiring caution, as shown in humans. Experimental manipulation of competitive contexts in primates reveals common mental processes involved in social judgment, and shows that access to valuable resources can be a sufficient cause for variations in group cohesion.     

Affiliation Between Aggressors and Third Parties Following Conflicts in Long-Tailed Macaques (Macaca fascicularis)

Studies on cercopithecine monkeys have shown that soon after an agonistic conflict, victims have increased rates of affiliation with the agressor—reconciliation—but not with other group members. Postconflict affiliation is thought to function to restore disturbed relationships and to reduce social tension. This study on a captive group of long-tailed macaques (Macaca fascicularis) is focused on postconflict affiliative behavior of the aggressor. Increased rates of contact between female aggressors and kin of the victim occurred, as well as between female aggressors and their own kin. Furthermore, there were increased rates of contact between aggressors—males and females—and other group members. The increase in contacts with the victim's kin was selective, i.e., it could not be ascribed to the increased contact tendency with group members in general, and was not a side effect of the aggressor's proximity to the victim due to reconciliation. The increase in contacts with own kin was not selective. The fact that male aggressors do not have increased postconflict contacts with their kin or with kin of the victim is in agreement with the notion that males are less integrated in the nepotistic matrilineal network than females are. The fact that studies by others that focused on the victim evidence no increase in postconflict contacts with kin of the opponent or with other group members may be explained by the aggressor's larger influence over the postconflict situation: to reduce social tension, it might be more effective to affiliate with the aggressor than with the victim. Our findings emphasize that conflicts influence the behavior of other monkeys besides the direct contestants and, thus, indicate that the disturbance of social homeostasis is a matter of concern for all group members.     

Clinical and Pathologic Features of Cynomolgus Macaques (Macaca fascicularis) Infected with Aerosolized Yersinia pestis

Since the anthrax attacks of 2001, the emphasis on developing animal models of aerosolized select agent pathogens has increased. Many scientists believe that nonhuman primate models are the most appropriate to evaluate pulmonary response to, vaccines for, and treatments for select agents such as Yersinia pestis (Y. pestis), the causative agent of plague. A recent symposium concluded that the cynomolgus macaque (Macaca fascicularis) plague model should be characterized more fully. To date, a well-characterized cynomolgus macaque model of pneumonic plague using reproducible bioaerosols of viable Y. pestis has not been published. In the current study, methods for creating reproducible bioaerosols of viable Y. pestis strain CO92 (YpCO92) and pneumonic plague models were evaluated in 22 Indonesian-origin cynomolgus macaques. Five macaques exposed to doses lower than 250 CFU remained free of any indication of plague infection. Fifteen macaques developed fever, lethargy, and anorexia indicative of clinical plague. The 2 remaining macaques died without overt clinical signs but were plague-positive on culture and demonstrated pathology consistent with plague. The lethal dose of plague in humans is reputedly less than 100 organisms; in this study, 66 CFU was the dose at which half of the macaques developed fever and clinical signs (ED₅₀), The Indonesian cynomolgus macaque reproduces many aspects of human pneumonic plague and likely will provide an excellent model for studies that require a macaque model.Yersinia pestis is the causative agent of plague. Likely more people worldwide have died from Y. pestis infections than from any other single infectious disease.^26,27 Bubonic plague, the most common form of the disease, results when the bacterium is inoculated into the skin, typically by means of flea bites. The resulting cutaneous infection spreads to local lymph nodes; the swollen lymph nodes are known as bubos and often serve as a source of systemic infection. Although less common, the bacterium also can spread by aerosol, causing pneumonic plague. Pneumonic plague can result from pulmonary spread of systemic infection or from deliberate dissemination and is associated with nearly 100% human mortality if left untreated. Y. pestis is susceptible to commonly available antibiotics if treatment begins soon after infection. However, depending on the route of infection, the time at which infection is confirmed is often too late for antibiotics to prevent significant morbidity or mortality.¹⁰ Because pneumonic plague is the form most likely to be seen in bioterrorism events,¹⁶ interest in animal models has arisen to support development of vaccines and improved therapeutics.Potential vaccines and therapeutic agents for plague must protect against the pneumonic disease, but contemporary published data regarding disease pathogenesis using aerosolized Y. pestis pathogenesis in nonhuman primates are scant.^4,9,21,23,24 In the United States, when vaccine or antibiotic efficacy cannot be evaluated in humans, an animal species that is reasonably expected to recapitulate human disease must be used.⁹ For many biothreat agents such as plague, a nonhuman primate model often is required. Although some laboratories have examined the cynomolgus macaque model of aerosolized plague briefly,¹ no published reports fully characterize this model. Published studies have examined plague in the African green monkey or vervet (Chlorocebus spp., formerly Cercopithecus aethiops) and rhesus macaque (Macaca mulatta).¹ Vervets reportedly are more sensitive to plague than are macaques,^4,24 such that some vervets are susceptible to infection with vaccine strains, casting some doubt on applicability of this species for plague studies.¹ The disease in rhesus macaques differs from that in humans in that rhesus macaques frequently develop disseminated intravascular coagulation (DIC) and chronic pneumonia as a result of pneumonic plague while humans usually develop acute pneumonia without DIC.^1,7Many participants at a recent symposium sponsored by the Food and Drug Administration and National Institute of Allergy and Infectious Disease endorsed the development of a cynomolgus macaque pneumonic plague model to support plague therapeutic and vaccine studies.⁸ The current study was undertaken to evaluate the Indonesian cynomolgus macaque as a model of aerosolized Y. pestis Colorado 92 (YpCO92) for subsequent vaccine and therapeutic trials. We also sought to determine whether fever development could be used to determine a humane endpoint to the study, as an alternative to LD₅₀ methods.     

Anxiety Level Predicts Post-Conflict Behaviour in Wild Japanese Macaques (Macaca fuscata yakui)

Reconciliation (i.e. the post-conflict exchange of friendly behaviour between former opponents) functions to control for the detrimental effects that aggression may have on social relationships. Studies conducted so far have investigated intra-individual sources of variation in post-conflict behaviour, showing that animals have a stronger increase in anxiety and are more likely to reconcile after conflicts with valuable partners, such as kin. Much less attention has been given to how differences between individuals in emotional profiles affect post-conflict behaviour. Our aim was to analyse whether inter-individual differences in baseline anxiety levels predicted the magnitude of the increase in anxiety following a conflict and the occurrence of reconciliation. We collected data on two groups of wild Japanese macaques ( Macaca fuscata yakui ). Animals having a higher baseline level of anxiety had a more dramatic anxious response following a conflict while controlling for a series of factors (e.g. relationship quality between opponents). These more anxious animals were also less likely to reconcile than more relaxed individuals. Therefore, more anxious animals face some social costs by being less able to cope with the post-conflict condition. We propose that differences in anxiety levels may be interpreted as tradeoffs between benefits and costs across conditions. For example, more anxious animals, who are less able to reconcile conflicts, might also be less exploratory and thus face a lower risk to eat unknown, poisonous food.     

Inequity aversion in relation to effort and relationship quality in long-tailed Macaques (Macaca fascicularis)

Social animals may employ evolved implicit rules to maintain a balance between cooperation and competition. Inequity aversion (IA), the aversive reaction to an unequal distribution of resources, is considered such a rule to avoid exploitation between cooperating individuals. Recent studies have revealed the presence of IA in several nonhuman species. In addition, it has been shown that an effort is crucial for this behavior to occur in animals. Moreover, IA may well depend on the partner's identity. Although dominant individuals typically monopolize food, subordinate individuals obtain less preferred food and usually do not protest. Furthermore, "friends" may pay less attention to equity than "nonfriends." We tested whether long-tailed macaques show IA with different cost-benefit ratios. In addition, we determined whether IA depends on relationship quality (RQ). Dominant subjects expressed IA only when a small effort was required. At a very large effort, however, long-tailed macaques did not show IA, possibly owing to bottom effects on the number of rewards they aim to receive. Moreover, and contrary to our predictions, an individual's inequity response was similar when tested with a "friend" or a "nonfriend." Therefore, we conclude that long-tailed macaques show IA only in conditions of moderate effort, yet that IA seems independent of RQ. Furthermore, IA may not be domain specific. Altogether, IA may be a trait present in all species that habitually cooperate, independent of their social organization.     

笼养雌性短尾猴月经周期及性行为

在多雄多雌的灵长类社会中,成年雌雄个体的性行为并不局限于雌性受孕期,但仍认为性行为在受孕期最为活跃.对于雌性隐藏发情的灵长类物种,雌雄个体的性行为与雌性月经周期的相关性尚不清楚.本研究以短尾猴(Macaca thibetana)为研究对象,研究雌性隐藏发情灵长类的性行为与月经周期阶段的关系.在短尾猴繁殖季节,从2019...     

Mitogenomic phylogeny of the common long-tailed macaque (Macaca fascicularis fascicularis)

Background

Long-tailed macaques (Macaca fascicularis) are an important model species in biomedical research and reliable knowledge about their evolutionary history is essential for biomedical inferences. Ten subspecies have been recognized, of which most are restricted to small islands of Southeast Asia. In contrast, the common long-tailed macaque (M. f. fascicularis) is distributed over large parts of the Southeast Asian mainland and the Sundaland region. To shed more light on the phylogeny of M. f. fascicularis, we sequenced complete mitochondrial (mtDNA) genomes of 40 individuals from all over the taxon’s range, either by classical PCR-amplification and Sanger sequencing or by DNA-capture and high-throughput sequencing.

Results

Both laboratory approaches yielded complete mtDNA genomes from M. f. fascicularis with high accuracy and/or coverage. According to our phylogenetic reconstructions, M. f. fascicularis initially diverged into two clades 1.70 million years ago (Ma), with one including haplotypes from mainland Southeast Asia, the Malay Peninsula and North Sumatra (Clade A) and the other, haplotypes from the islands of Bangka, Java, Borneo, Timor, and the Philippines (Clade B). The three geographical populations of Clade A appear as paraphyletic groups, while local populations of Clade B form monophyletic clades with the exception of a Philippine individual which is nested within the Borneo clade. Further, in Clade B the branching pattern among main clades/lineages remains largely unresolved, most likely due to their relatively rapid diversification 0.93-0.84 Ma.

Conclusions

Both laboratory methods have proven to be powerful to generate complete mtDNA genome data with similarly high accuracy, with the DNA-capture and high-throughput sequencing approach as the most promising and only practical option to obtain such data from highly degraded DNA, in time and with relatively low costs. The application of complete mtDNA genomes yields new insights into the evolutionary history of M. f. fascicularis by providing a more robust phylogeny and more reliable divergence age estimations than earlier studies.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1437-0) contains supplementary material, which is available to authorized users.     

Social Behavior of Captive Indochinese and Insular Long-Tailed Macaques (Macaca fascicularis) Following Transfer to a New Facility

There are measurable differences in behavior, physiology, social organization, and geographic distribution within and between various species of macaques. We collected information on the social behavior of captive Macaca fascicularis from Indochina and island populations after they had been transferred to a new environment and new social groups. While some changes in behavior occurred over time, we found no decrease in high levels of agonistic behaviors. We interpret this finding in light of previous research reporting that long-tailed macaques show low levels of habitatuation to novelty and are highly aroused in comparison to other macaque species. We found predictable differences in behavior for males, females, and infants, in which infants played more, females had higher levels of contact proximity to other individuals, and males exhibited more sexual and threat behavior. A comparison of social behavior in long-tailed macaques from different origins indicate that Indochinese macaques are generally less affiliative and Indochinese males are more aggressive than their insular counterparts. Differences among macaque species, and within the fascicularis-group, should be considered in management of captive colonies and when interpreting research data.     

Influence of Climatic Factors on Pneumocys Carriage within a Socially Organized Group of Immunocompetent Macaques (Macaca fascicularis)

ABSTRACT. As monkeys-derived Pneumocystis is closely related to P. jirovecii , simian populations should be considered as valuable models for the understanding of the epidemiology of human pneumocystosis. In the present study, the impact of environmental factors on the carriage of Pneumocystis was evaluated in socially organized group of immunocoinpetent macaques (Macuca fascicularis). The tribe, maintained in partial release al the Primatology Center of Strasbourg in France, comprised 29 animals at the end of the study. From December 2000 to November 2002, deep nasal swab samples were collected monthly from each animal under general anaesthesia. The presence of Pneurmocystis DNA was assessed by nested PCR of mtLSU rRNA gene. No case of pneumocystosis was reported during the study. Pneumocystis DNA was detected in 166 out 01 481 swab samples examined (34.5%). The number of macaques with detectable Pneumocystis DNA was highly variable from one month to another. However, Pneumocystis carriage was clearly correlated to the mean precipitation rates.