The range of action of the mother and the avoidance of big novel objects in long-tailed macaques

Most surrogate-reared long-tailed macaques persistently avoid a big novel object, whereas most mother-reared subjects approach it. A striking difference between these attachment figures is that the mothers moved about with their infants, whereas the surrogates were fixed to the wall In this experiment, we aimed to find out whether mobility of the attachment figure plays a part in the development of an infant’s responses to big novel objects. We studied the effects of mobility of the attachment figure by restraining mothers in their range of action. We confined mothers of the experimental group in a small part of the home cage. Their infants could leave the cage in which their mothers were restrained. Infants that were growing up with unrestrained mothers made up the control group. At two different ages all infants encountered a big novel object. We used two different objects. We found that the range of action of the mother did not significantly affect the responses of infants to big novel objects. As in the previous studies, most of the mother-reared monkeys approached the objects. The age at which an infant was first exposed to an object did not significantly affect its behavior toward it. Further, the two different objects evoked the same reactions.     

Aggression and peripheralization in subadult male long-tailed macaques in Singapore

Aggression and peripheralization between adult and subadult male macaques have been postulated as proximate causes for dispersal, but empirical evidence for this relationship is scarce. To investigate the level of aggression and peripheralization experienced by subadult males, we conducted focal animal and scan sampling of two long-tailed macaque (Macaca fascicularis) groups in the highly anthropogenic environment of Singapore’s Central Nature Reserve. We followed two subadult males each in two groups and compared (1) aggression between subadult and adult males and (2) peripheralization measured by (a) greater interindividual distances, (b) more noninteractive behaviors, and (c) fewer interactive behaviors. After 72 focal hours, results suggest varying levels of peripheralization and consistently low levels of aggression among all four males. Data herein call into question the role of aggression in intragroup interactions. Differences in affiliation patterns appear to be core factors in determining the individual degree of peripheralization. Ultimately, strategic choices related to an individual’s place within the natal group (e.g., affiliations, rank of relatives) may be important to cost–benefit assessments; these choices have significant implications in both the short term (i.e., dispersal timing) and long term (i.e., reproductive success). This study is a first step toward understanding macaque behavior in anthropogenic environments; further exploration is needed to anticipate how landscape changes might influence macaque dispersal patterns. Greater understanding will come from recognition that social mechanisms are highly individualized and constantly dynamic, especially for highly cognitive, social species, and in ever increasingly dynamic anthropogenic environments.     

The effects of two novel objects on the behavior of singly caged adult rhesus macaques.

Six female and six male adult rhesus macaques were given sticks and nylon balls as an attempt at simple cage enrichment. A latin square design was used to compare behavior during separate 4-week periods with each object and during a control period with no object. Frequency and duration of 15 different behaviors were recorded. Resting was the most common activity which decreased slightly in duration when the stick or nylon ball was present (P less than 0.02). The mean duration of stick use was longer than that of the nylon ball (P less than 0.01). No other behaviors changed significantly, including the frequency of abnormal behaviors such as self-abuse, stereotypic acts, and bizarre postures. Generally, these objects were used infrequently and led to few changes in the behavior of singly-caged adult rhesus macaques. However, they did appear to stimulate activity for some individuals.     

Conflict,displacement activities,and menstrual cycle in long-tailed macaques

This study was aimed at testing whether the female menstrual cycle is associated with changes in social tension experienced by eight heterosexual pairs of long-tailed macaques (Macaca fascicularis). Displacement activities were considered as a behavioral measure of social tension and recorded during the periovulatory and the menstrual flow phases of the cycle. While male yawning and body shake underwent nonsignificant increases, male autogrooming and scratching increased significantly during the periovulatory phase. Female displacement activities did not show any significant difference between the two phases. Male and female socio-sexual behavior was not affected by the menstrual cycle. These results suggest that the male conflictual state, but not the female one, is affected by female menstrual cycle.     

Survey of the long-tailed macaques introduced onto Tinjil Island,Indonesia

From February 1988 though June 1990, 475 adult long-tailed macaques (Macaca fascicularis) were released on Tinjil Island to establish a breeding program that will provide monkeys for biomedical research while contributing to Indonesia's primate conservation efforts. A survey was conducted during the summer of 1990 to assess the status of the island's population. Basic demographic data were consistent with those from other field studies of long-tailed macaques, and estimates of reproductivity suggest a successful breeding program. The facility established on Tinjil Island should serve as a useful model for future primate resource and conservation programs. © 1993 Wiley-Liss, Inc.     

Positional behavior of long-tailed macaques (Macaca fascicularis) in northern Sumatra

Although the majority of extant primates are described as "quadrupedal," there is little information available from natural habitats on the locomotor and postural behavior of arboreal primate quadrupeds that are not specialized for leaping. To clarify varieties of quadrupedal movement, a quantitative field study of the positional behavior of a highly arboreal cercopithecine, Macaca fascicularis, was conducted in northern Sumatra. At least 70% of locomotion in travel, foraging, and feeding was movement along continuous substrates by quadrupedalism and vertical climbing. Another 14-25% of locomotion was across substrates by pronograde clambering and vertical clambering. The highest frequency of clambering occurred in foraging for insects, and on the average smaller substrates were used in clambering than during quadrupedal movement. All postural behavior during foraging and feeding was above-substrate, largely sitting. Locomotion across substrates requires grasping branches of diverse orientations, sometimes displaced away from the animal's body. The relatively low frequency of across-substrate locomotion appears consistent with published analyses of cercopithecoid postcranial morphology, indicating specialization for stability of limb joints and use of limbs in parasagittal movements, but confirmation of this association awaits interspecific comparisons that make the distinction between along- and across-substrate forms of locomotion. It is suggested that pronograde clambering as defined in this study was likely a positional mode of considerable importance in the repertoire of Proconsul africanus and is a plausible early stage in the evolution of later hominoid morphology and locomotor behavior.     

Morphology and somatometric growth of long-tailed macaques (Macaca fascicularis fascicularis) in Singapore

Crab-eating, or long-tailed, macaques [ Macaca fascicularis (Raffles, 1821)] have been studied extensively throughout their distribution in South and South-east Asia. Despite this extensive body of research, the island population of long-tailed macaques from Singapore remains virtually undescribed. In the present study, we compare the morphometric variability and patterns of growth observed in a population sample from Singapore with a composite sample from Thailand, north of the Isthmus of Kra. The results of our analyses indicate that there are statistically significant differences between the two populations in adult size and shape. For both males and females, the Singapore population is smaller than the Thai population. Relative to body length, the Singapore macaques exhibit significantly longer tails, and, relative to cranial length, they exhibit significantly more narrow faces than the Thai macaques. Although levels of sexual dimorphism for most morphometric traits are very similar, indicating similar levels of male–male competition for females, the Singapore males exhibit a significantly larger testicular volume relative to body weight, suggestive of an alternative male reproductive strategy. In addition to adult somatometric size and shape, comparisons of growth patterns relative to age and body size reveal significant differences between the two population samples. Combined, these results suggest either that statistically significant differences in adult morphology and patterns of growth can occur in presumably reproductively cohesive subspecies, or the Singapore macaques may be taxonomically distinct.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 675–694.     

The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand

BACKGROUND: Long-tailed and rhesus macaques are widely used in biomedical research; therefore, the known blood group is important. METHODS: The human-type ABO blood group was determined in wild or semi-wild long-tailed and rhesus macaques in Thailand. A total of 729 long-tailed and 160 rhesus macaques from 20 localities were temporarily caught. RESULTS: The frequency profiles of blood groups, calculated by averaging the frequency of each troop in long-tailed and rhesus macaques, were AB > O > B > A at 29.6%, 27.4%, 27.2%, and 15.8%, and B > AB > A > O at 39.6%, 33.4%, 18.2%, and 8.8%, respectively. Irrespective of locality, the frequencies were AB > O > B > A of 29.6%, 28.0%, 24.4%, and 18.0%, and AB > B > A > O of 37.5%, 28.7%, 26.9%, and 6.9%, respectively, for all long-tailed and rhesus macaques. The frequency profile of blood groups in Thai rhesus macaques was somewhat similar to that in the parapatric long-tailed macaques; however, it was different from other rhesus populations where only group B was detected. CONCLUSIONS: Our data support the hypothesis that Indochinese rhesus macaques are hybrids between rhesus and long-tailed macaques in the past.     

Small-scale variability in a mosaic tropical rainforest influences habitat use of long-tailed macaques

Pristine habitats have generally been considered to be the most important ecological resource for wildlife conservation, but due to forest degradation caused by human activities, mosaics of secondary forests have become increasingly prominent. We studied three forest types in a mosaic tropical forest consisting of short secondary forest (SS), tall secondary forest (TS) and freshwater swamp forest (SF). These forests differed in stand structure and floristic composition, as well as phenological productivity of fruits, flowers and young leaves. We examined habitat use of long-tailed macaques (Macaca fascicularis) in relation to indices of phenological activity. The macaques used the SS for feeding/foraging more than the TS and the SF. This was because the SS had higher productivity of fruit, which is a preferred food resource for macaques. Stem densities of young leaves in the SS and the TS also influenced habitat use, as they provided more clumped resources. Use of SF was limited, but these forests provided more species-rich resources. Our results showed that M. fascicularis responded to small-scale variability in phenological activity between forest types found in a heterogeneous mosaic forest, with young secondary regrowth forests likely providing the most important food resources. Mosaic landscapes may be important as they can buffer the effects of temporal food resource variability in any given forest type. In our increasingly human-altered landscapes, a better understanding of the role of secondary forest mosaics is crucial to the conservation and management of wildlife habitats and the animals they support.     

Stimulus enhancement and spread of a spontaneous tool use in a colony of long-tailed macaques

In a captive group of long-tailed macaques, tool-using behavior by a single competent individual had a significant effect on the synchronous manipulative behavior of naïve animals. Group members engaged in manipulations on the same object class more frequently during times when the model was working than when it was not. The form of their behavior, however, in no way resembled the technique used by the model. All three animals that later became successful tool users were among the few subjects that exhibited a significant increase in manipulations on the same object class while the model was working. Possible causal relationships between this stimulus enhancement and the transmission of the new behavior to other group members are analyzed and discussed.     

Relatedness of matrilines,dispersing males and social groups in long-tailed macaques (Macaca fascicularis).

Genealogical relatedness is thought to be an important causal factor in the evolution of cooperation. We inferred relatedness on the basis of 11 blood protein markers using the Queller and Goodnight index of relatedness in a macaque population with long-term demographic records. This estimate reflected independently determined pedigree relationships in our data set. Mean relatedness among all members of a social group was 0.10 but much higher levels of relatedness (0.30-0.47) were found among the members of matrilineal families with a high or intermediate social rank. Groups of dispersing males that had been born into the same social group were sometimes closely related (0.43 and 0.58), but they could also be less related (0.08). We found that the pattern of distribution of relatedness was associated with gene flow and differential reproduction in males, rather than with group fission and the presence of geographical barriers.     

The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques,Macaca fascicularis

Demographic changes were recorded throughout a 12-year period for three social groups ofMacaca fascicularis in a natural population at Ketambe (Sumatra, Indonesia). We examined the prediction that females' lifetime reproductive success depended on dominance rank and group size. Average birth rate was 0.53 (184 infants born during 349 female years). For mature females (aged 8–20 yr) birth rate reflected physical condition, being higher in years with high food availability and lower in the year following the production of a surviving infant. High-ranking females were significantly more likely than low-ranking ones to give birth again when they did have a surviving offspring born the year before (0.50 vs 0.26), especially in years with relatively low food availability (0.37 vs 0.10). Controlled comparisons of groups at different sizes indicate a decline in birth rate with rroup size only once a group has exceeded a certain size. The dominance effect on birth rate tended to be strongest in large groups. Survival of infants was rank-dependent, but the survival of juveniles was not. There was a trend for offspring survival to be lower in large groups than in mid-sized or small groups. However, rank and group size interacted, in that rank effects on offspring survival were strongest in large groups. High-ranking females were less likely to die themselves during their top-reproductive years, and thus on average had longer reproductive careers. We estimated female lifetime reproductive success based on calculated age-specific birth rates and survival rates. The effects of rank and group size (contest and scramble) on birth rate, offspring survival, age of first reproduction for daughters, and length of reproductive career, while not each consistently statistically significant, added up to substantial effects on estimated lifetime reproductive success. The group size effects explain why large groups tend to split permanently. Since females are philopatric in this species, and daughters achieve dominance rank positions similar to their mother, a close correlation is suggested between the lifetime reproductive success of mothers and daughters. For sons, too, maternal dominance affected their reproductive success: high-born males were more likely to become top-dominant (in another group). These data support the idea that natural selection has favored the evolution of a nepotistic rank system in this species, even if the annual benefits of dominance are small.     

Effects of 13-cis-retinoic acid on hindbrain and craniofacial morphogenesis in long-tailed macaques (Macaca fascicularis)

Hindbrain and craniofacial development during early organogenesis was studied in normal and retinoic acid-exposed Macaca fascicularis embryos. 13-cis-retinoic acid impaired hindbrain segmentation as evidenced by compression of rhombomeres 1 to 5. Immunolocalization with the Hoxb-1 gene product along with quantitative measurements demonstrated that rhombomere 4 was particularly vulnerable to size reduction. Accompanying malformations of cranial neural crest cell migration patterns involved reduction and/or delay in pre- and post-otic placode crest cell populations that contribute to the pharyngeal arches and provide the developmental framework for the craniofacial region. The first and second pharyngeal arches were partially fused and the second arch was markedly reduced in size. The otocyst was delayed in development and shifted rostrolaterally relative to the hindbrain. These combined changes in the hindbrain, neural crest, and pharyngeal arches contribute to the craniofacial malformations observed in the retinoic acid malformation syndrome manifested in the macaque fetus.     

Effects of excess selenomethionine on selenium status indicators in pregnant long-tailed macaques (Macaca fascicularis)

Forty pregnant long-tailed macaques were treated daily for 30 d with 0, 25, 150 or 300 μg selenium as L-selenomethionine/kg body weight. Erythrocyte and plasma selenium and glutathione peroxidase specific activities, hair and fecal selenium, and urinary selenium excretion were increased by and were linearly related to L-selenomethionine dose. Hair selenium was most sensitive to L-selenomethionine dose, with an 84-fold increase in the 300 μg selenium/(kg-d) group relative to controls (r=0.917). Daily urinary selenium excretion (80-fold,r=0.958), plasma selenium (22-fold,r=0.885), erythrocyte selenium (24-fold,r=0.920), and fecal selenium (18-fold,r=0.911) also responded strongly to L-selenomethionine. Erythrocyte and plasma glutathione peroxidase specific activities increased 154% and 69% over controls, respectively. Toxicity was associated with erythrocyte selenium >2.3 μg/mL, plasma selenium >2.8 μg/mL, and hair selenium >27 μg/g. Plasma, erythrocyte, and hair selenium concentrations may be useful for monitoring and preventing the toxicity of L-selenomethionine administered to humans in cancer chemoprevention trials.     

Intergroup variation in robbing and bartering by long-tailed macaques at Uluwatu Temple (Bali,Indonesia)

Robbing and bartering (RB) is a behavioral practice anecdotally reported in free-ranging commensal macaques. It usually occurs in two steps: after taking inedible objects (e.g., glasses) from humans, the macaques appear to use them as tokens, returning them to humans in exchange for food. While extensively studied in captivity, our research is the first to investigate the object/food exchange between humans and primates in a natural setting. During a 4-month study in 2010, we used both focal and event sampling to record 201 RB events in a population of long-tailed macaques (Macaca fascicularis), including four neighboring groups ranging freely around Uluwatu Temple, Bali (Indonesia). In each group, we documented the RB frequency, prevalence and outcome, and tested the underpinning anthropogenic and demographic determinants. In line with the environmental opportunity hypothesis, we found a positive qualitative relation at the group level between time spent in tourist zones and RB frequency or prevalence. For two of the four groups, RB events were significantly more frequent when humans were more present in the environment. We also found qualitative partial support for the male-biased sex ratio hypothesis [i.e., RB was more frequent and prevalent in groups with higher ratios of (sub)adult males], whereas the group density hypothesis was not supported. This preliminary study showed that RB is a spontaneous, customary (in some groups), and enduring population-specific practice characterized by intergroup variation in Balinese macaques. As such, RB is a candidate for a new behavioral tradition in this species.     

Status referents in long-tailed macaques (Macaca fascicularis): Precursors and effects of a female rebellion

The antecedents and consequences of a change in status in the female line have been documented in the course of an ongoing study of a captive colony ofMacaca fascicularis. A conjunction of two events appears to have been a cause of the timing. The first is the maturation of the eldest female offspring of the subordinate lineage, and the second the insertion of an intrauterine device into the mother of that lineage. These changes made these two females simultaneously sexual associates of the adult male, while the dominant female of the other lineage was still pregnant. In the course of these events the maturing sub-adult female of the subordinate lineage underwent the most dramatic change of status, eventually rising from the lowest position to that of alpha female. The complex changes which heralded this alternation in status are described in terms of the referent relations and alliances which were evolving in the group. The word “revolution” is reserved for a change in the type of social structure brough about by insurrection: rebellion occurs when insurrection changes the position of the individuals in a structure which is itself left unchanged -vide, Webster’s English Dictionary.     

Acquisition of object-robbing and object/food-bartering behaviours: a culturally maintained token economy in free-ranging long-tailed macaques

The token exchange paradigm shows that monkeys and great apes are able to use objects as symbolic tools to request specific food rewards. Such studies provide insights into the cognitive underpinnings of economic behaviour in non-human primates. However, the ecological validity of these laboratory-based experimental situations tends to be limited. Our field research aims to address the need for a more ecologically valid primate model of trading systems in humans. Around the Uluwatu Temple in Bali, Indonesia, a large free-ranging population of long-tailed macaques spontaneously and routinely engage in token-mediated bartering interactions with humans. These interactions occur in two phases: after stealing inedible and more or less valuable objects from humans, the macaques appear to use them as tokens, by returning them to humans in exchange for food. Our field observational and experimental data showed (i) age differences in robbing/bartering success, indicative of experiential learning, and (ii) clear behavioural associations between value-based token possession and quantity or quality of food rewards rejected and accepted by subadult and adult monkeys, suggestive of robbing/bartering payoff maximization and economic decision-making. This population-specific, prevalent, cross-generational, learned and socially influenced practice may be the first example of a culturally maintained token economy in free-ranging animals.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates''.     

Post-conception mating in wild long-tailed macaques (Macaca fascicularis): characterization, endocrine correlates and functional significance

In many anthropoid primates, mating activity is not restricted to the ovarian cycle but also occurs during pregnancy. Although it has been suggested that the main function of this post-conception mating is to confuse paternity, studies showing whether or not male primates can distinguish between the fertile phase of the conception cycle (FPCC) and the period of peak post-conception mating (peak PCM) are almost non-existent. Here, we examine whether the pattern of female sexual traits (specific sexual behaviors, sexual swelling) and female attractiveness to males differ between FPCC and peak PCM in 6 wild female long-tailed macaques. We also use fecal hormone analysis to investigate whether female traits during peak PCM are related to changes in female sex hormones. All females exhibited a distinct period of heightened mating activity around days 45-60 of gestation. During peak PCM, swelling size and frequency of female solicitations (but not reaching back) were significantly correlated with changes in the estrogen to progestogen ratio. Swelling size, frequency of female sexual behaviors and copulations and proportion of male-initiated copulations and ejaculations were not significantly different between FPCC and peak PCM. Although males spent significantly less time consorting females during peak PCM, all (particularly low-ranking and non-resident males) invested heavily in terms of reproductive costs associated with mate-guarding and mating during pregnancy. We conclude that post-conception mating in wild long-tailed macaques is not merely a by-product of endocrine changes and devoid of adaptive function. Our results more strongly support the hypothesis that it may form part of a female reproductive strategy to confuse paternity, which appears to apply particularly to low-ranking and extra-group males.     

The effects of twinning on mother—Offspring behavior in range beef cattle

Methods to increase the productivity of beef cattle include induced twinning and multiple fostering of calves on nurse cows, but little is known about the capacity of cows to rear more than one calf in a rangeland environment.Eight single and 14 twin calves and their mothers were studied in a 30.4-ha enclosure in a California rangeland environment from 2 to 20 weeks following parturition. Data were obtained on ingestive, grooming, agonistic, play and sexual behaviors, as well as spatial proximity of calves to mothers and peers.Initially, twins spent more time suckling their mothers than did single calves (presumably due to insufficient milk intake), but later adapted by utilizing natural forage and obtaining milk from alien cows. By 15–20 weeks of age, twins were suckling their dams for less than one-quarter of the time spent at 3–6 weeks, whereas the suckling time of single calves did not decline. Thus, twins may experience a natural early weaning from mother's milk.The hypothesis that mother—Offspring bonds are weaker with twins than with singles was supported by the fact that mothers bearing twins groomed their offspring less than mothers with singles, and twins were normally found at greater distances from their mothers than singles.Most long-distance cow—Calf separations resulted from the cow moving to feed or to obtain water. Reunion of mother and young depended on auditory communication; the calf normally traversed most of the intervening distance.