Effects of proximity and activity on visual and auditory monitoring in wild Japanese macaques

Group-living primates monitor group members to maintain the spatial cohesiveness of the group. We examined the possibility that visual scanning (turning the head for more than 3 sec) and contact calls (coo calls) function as visual and auditory monitoring behaviors to avoid separation from group members in wild Japanese macaques. The rate of visual scanning increased as proximity to group members decreased and as mobile activities (foraging and moving) increased, compared with immobile activities (resting and grooming). However, the rate of contact calls varied differently with proximity and activities. During resting and moving, the rate of contact calls increased as proximity decreased. In contrast, the rate increased with closer proximity during feeding. Visual scanning during all activities and contact calls during resting and moving increased when the group members were likely to spread over a larger area, suggesting that these behaviors functioned as monitoring of group members to avoid separation from the group. Contact calls also increased when the group members stayed in close proximity during foraging, suggesting that this behavior was also associated with competitive situations. Contact calls may also function to ease tension or maintain distance to avoid conflict in competitive situations.     

Adjustment of Temporal Call Usage During Vocal Exchange of Coo Calls in Japanese Macaques

Japanese macaques (Macaca fuscata) exchange coo calls with group members to maintain contact. I examined the relationship between the distance between group members and (1) the latency of vocal responses to spontaneous calls, and (2) the latency of spontaneous call repetition in the absence of vocal responses. After a subject monkey's spontaneous call, the latency of vocal response by another group member was longer when the subject was farther from the group members than when the subject was near the group members. Furthermore, subject repeated calls with longer intervals in the absence of vocal response, which suggests that they wait longer for the vocal responses of other group members when the expected response latency is longer. These results reveal that Japanese macaques flexibly alter the timing of their calls based on others’ vocal responses.     

Cross-Sectional and Longitudinal Studies of the Development of Group Differences in Acoustic Features of Coo Calls in Two Groups of Japanese Macaques

Japanese macaques, Macaca fuscata, frequently utter coo calls to maintain vocal contact. Cross‐sectional and longitudinal comparisons were conducted on the acoustic features of coo vocalizations of two groups of M. fuscata, Yakushima and Ohirayama groups, to explore the possibility of vocal plasticity. These two groups derive from the same local population but have been separated for more than 34 yr. The Yakushima group is non‐provisioned, while the Ohirayama group is provisioned. Initially, coo calls in the two groups were compared cross‐sectionally in females ranging from 0 to 18 yr. Mean values of the four variables studied (start, end, maximum, and minimum frequencies) were consistently lower in all age groups of the Ohirayama individuals compared with the Yakushima individuals. Secondly, longitudinal comparisons were conducted on individuals in the 1–4 yr after birth. Mean values of the five frequency variables studied (start, end, maximum, minimum and average frequencies) were again consistently lower in all age groups of Ohirayama compared with Yakushima individuals, although mean values of both groups gradually declined with an increase in age. Inter‐group differences were significant at all ages in minimum frequency and at the first, second and third years in start frequency. Longitudinal comparisons of individuals aged 4–11 mo were also conducted. Regarding the four variables that differed between the two groups in the cross‐sectional study, the mean values of minimum and start frequency did not differ significantly between the two groups at 4–5 mo, but were significantly lower in Ohirayama individuals aged 7–8 and 9–11 mo. Although provisioning may have had an effect on the weight difference between the groups, and consequently on vocalization frequency, these results suggest that the inter‐group differences in coo call features form approximately 6–7 mo after birth as a result of vocal plasticity.     

Factors Affecting Proximity Among Members of a Wild Group of Moor Macaques During Feeding,Moving, and Resting

We studied the effects of kinship, age, sex, and other factors on patterns of spatial proximity among group members in a wild group of moor macaques (Macaca maurus) in Sulawesi, Indonesia. We assessed the importance of each factor via multiple linear regression analyses. Moor macaques stay close to their matrilineal relatives more frequently when the group moves or rests than when they feed. Subjects of similar age, sex, or rank tended to stay close to each other. Females were in the proximity of females with newborn infants regardless of the phase of activity of the group. Kinship may have less effect on proximity during feeding in moor macaques than in Japanese macaques. Weak effects of kinship during feeding may result from weak contest competition for food within the group.     

The significant features of Japanese macaque coo sounds: a psychophysical study

Japanese macaques, Macaca fuscata, were trained with a positive reinforcement operant procedure to discriminate smooth early high and smooth late high coo sounds recorded during Green's (1975) field study of the speices' vocal repertoire. Subjects labelled the various tokens by maintaining contact with a response device for calls from one category and by breaking contact for those of the second call type. After the completion of discrimination training, the generalization of the operant behaviour to novel natural and synthetic vocalizations was measured. Initial generalization tests established that macaques would respond appropriately both to natural vocalizations and to computer-synthesized prototypes representing the smooth early high-smooth late high contrast. In subsequent tests, individual acoustic features were removed from the synthetic prototypes to determine the minimal elements of functional coo sounds. These tests suggested that those sounds are distinguished by the predominant direction of their frequency change which, in turn, is determined by the temporal position of their highest frequency.     

Effects of contextual and social variables on contact call production in free-ranging ringtailed lemurs (Lemur catta)

Ringtailed lemurs (Lemur catta)often emit a characteristic vocalization when resting as a troop. This “meow call” is believed to serve an intragroup contact function. I investigated the effects of behavioral context and proximity on call production and acoustic features of the vocalization in a free-ranging troop in the Berenty Reserve, Madagascar. When group members were dispersed, the meow call was given frequently, and the acoustic features of the call probably increased the locatability of the emitter. I evaluated social relationships among the troop members from grooming interactions and spacing data. I also studied the call exchange network among the troop members, the results of which indicate that calls are exchanged between the two subgroups of females, which they connect.     

Vocal communication of tonkean macaques in confined environments

Vocal recordings of one semi-free-ranging group and one captive group of Tonkean macaques (Macaca tonkeana) were used to establish the vocal repertoire of the species. Only the alpha male of the groups uttered a very distinctive loud call. Localization variants of coo calls were found. Alarm calls given by this species were acoustically similar to those by Japanese, rhesus, and long-tailed macaques (M. fuscata, M. mulatta, andM. fascicularis). Adult females uttered a specific variant of vocalizations during sexual morphological changes. The repertoire of agonistic vocalizations was more variable than that of any other macaque species investigated. These characteristics were discussed with reference to previous studies on vocalizations of macaque species.     

Factors Affecting Acoustic Variation in Barbary-macaque (Macaca sylvanus) Disturbance Calls

Semi-free-ranging Barbary macaques (Macaca sylvanus) were observed to utter distinctive calls after disturbances in the surroundings (e.g. presence of a predator, occurrence of some unusual phenomenon). These calls differed from calls given in other contexts. Most of these calls were uttered in a serial manner, some of which lasted as long as the corresponding context. The aim of this study was to determine the object-related specificity of calls and variation of acoustic parameters within a call series. The analysis revealed that acoustic features of calls varied among contexts. Within one apparently homogeneous context, both temporal and frequency characteristics shifted gradually. Furthermore, the disturbance calls clearly differed between individuals. To examine the disturbance calls' meaning, playback experiments were conducted in which alarm calls and disturbance calls were presented. After playback of an alarm call, subjects typically showed an escape response, whereas, in response to disturbance calls, they most often scanned the surroundings. Juvenile animals generally showed stronger responses than adults.     

Production and perception of sex differences in vocalizations of Wied's black‐tufted‐ear marmosets (Callithrix kuhlii)

Males and females from many species produce distinct acoustic variations of functionally identical call types. Social behavior may be primed by sex‐specific variation in acoustic features of calls. We present a series of acoustic analyses and playback experiments as methods for investigating this subject. Acoustic parameters of phee calls produced by Wied's black‐tufted‐ear marmosets (Callithrix kuhlii) were analyzed for sex differences. Discriminant function analyses showed that calls contained sufficient acoustic variation to predict the sex of the caller. Several frequency variables differed significantly between the sexes. Natural and synthesized calls were presented to male–female pairs. Calls elicited differential behavioral responses based on the sex of the caller. Marmosets became significantly more vigilant following the playback of male phee calls (both natural and synthetic) than following female phee calls. In a second playback experiment, synthesized calls were modified by independently manipulating three parameters that were known to differ between the sexes (low‐, peak‐, and end‐frequency). When end‐frequency‐modified calls were presented, responsiveness was differentiable by sex of caller but did not differ from responses to natural calls. This suggests that marmosets did not use end‐frequency to determine the sex of the caller. Manipulation of peak‐and low‐frequency parameters eliminated the discrete behavioral responses to male and female calls. Together, these parameters may be important features that encode for the sex‐specific signal. Recognition of sex by acoustic cues seems to be a multivariate process that depends on the congruency of acoustic features. Am. J. Primatol. 71:324–332, 2009. © 2008 Wiley‐Liss, Inc.     

Do Barbary macaques ‘comment’ on what they see? A first report on vocalizations accompanying interactions of third parties

Primates acquire knowledge about relationships of third parties and group structure by monitoring their conspecifics. We show that Barbary macaques (Macaca sylvanus) utter specific vocalizations while monitoring interactions of other group members. As they did not direct other behaviours to the interacting group members, we provisionally termed these vocalizations vocal comments. We investigated the acoustic properties of these comments and the social contexts in which they occurred. Most adult males and females of two studied groups produced low-amplitude calls when observing close contact interactions of other group members. The acoustic features of these calls varied with characteristics of the commented situation. Our results suggest that such calls might not be directed towards the agents of the commented situation, but towards other group members. The vocal comments may signal the callers awareness of the observed interaction and possibly attract the attention of others to the situation.     

Japanese Macaques Depend not Only on Neighbours but also on More Distant Members for Group Cohesion

A well‐known behavioural model for group aggregation is that an individual depends on a few neighbouring individuals to adjust its movement, such as departure (repulsion) from and approach (attraction) to neighbours. However, an individual may rely not only on a few closest neighbours, but also on more distant individuals, in a group of stable membership. We measured temporal changes in the local density of individuals around a focal individual and changes in distance to other focal individuals in a group of wild Japanese macaques to determine whether the macaques depended only on a few neighbours or also on more distant individuals for adjustments in cohesiveness. We used simultaneous focal animal sampling, with two observers recording the individuals' locations using a global positioning system (GPS), over three seasons. Numbers of individuals within 20 m from an animal tended to increase after 10 min when there were a small number of individuals around the animal. However, the number tended to decrease when there was a larger number of individuals. It remained similar when there were an intermediate number of individuals. The two focal animals tended to separate after 10 min when the interindividual distance was short. However, they tended to move closer when far apart. They remained a similar distance apart when they were at an intermediate distance. Contact calls, which are suggested to function as locating group members and keeping cohesiveness, were emitted more frequently when the distance between the two focal animals was very large in two seasons. However, the rate of contact calls was not influenced by the number of individuals within 20 m from an animal. These results suggest that individual Japanese macaques do not only rely on a few closest neighbours, but also rely on more distant group members. Japanese macaques may know the general whereabouts of the whole group, and when they stay at the periphery of the group, they may emit contact calls frequently and move towards the central zone so as not to become separated from the group.     

Effects of caller activity and habitat visibility on contact call rate of wild Japanese macaques (Macaca fuscata)

A major function of contact calls in nonhuman primates is to maintain spatial cohesion among individuals in a group. The risks of spatial/visual separation from the group are likely to affect auditory contact behavior, in particular by increasing the call rate. We tested whether the risk of separation influences coo call emission by investigating the variation in call rate among behavioral contexts in two wild populations of Japanese macaques (Macaca fuscata). We focused on caller activity and the degree of visibility within the habitat as primary potential factors mediating call rate. We first estimated the habitat visibility of the two research sites at Yakushima Island (YK) and Kinkazan Island (KZ), Japan. The habitat visibility of YK was significantly more restricted than that of KZ. We then compared the call rate of 20 adult and 12 juvenile female macaques between the two wild populations to examine the potential effects of environmental differences. Both populations had a lower call rate during grooming than during feeding and moving, which are behaviors associated to higher interindividual distances. The call rate of YK adult females was significantly greater than that of both juveniles and KZ adult females, independently of activity. The call rate increased as macaques matured in the YK population, but not in the KZ population, suggesting that different developmental processes involved in contact calling of the two populations. Our findings suggest that separation risk influences call rate, and also imply a possibility of social influence that social structure change effects on the call rates.     

Perception of female reproductive state from vocal cues in a mammal species

While acoustic signalling by males is known to affect male-male competition, mate attraction and the timing of ovulation, the extent to which sexual selection has shaped the evolution of female acoustic signals is poorly understood. Among mammals, experimental evidence indicates that females attract mating partners by using olfactory and visual signals to advertise their reproductive state. Whether or not males ascertain female reproductive state from vocal signals has, however, never been systematically tested. In this study, we use playbacks of recorded vocalizations to demonstrate that male Barbary macaques, Macaca sylvanus, can discriminate between female copulation calls given at different stages of the oestrous cycle, responding more strongly to those given around the time when conception is most likely to occur. Acoustic analysis suggests that the mean dominant frequency of call units and a number of temporal parameters could provide males with the information necessary to discern the proximity of ovulation in this way Our results provide the first experimental evidence that the calls of female mammals may contain information on reproductive state, which males can perceive and use in such a way as to increase their reproductive success.     

Psycholinguistic analyses of alarm calls of Japanese monkeys (Macaca fuscata fuscata)

Alarm and estrous calls emitted by Japanese macaques were recorded and analyzed in the Arashiyama West and East groups. Their responses to natural calls as well as to synthesized versions varying in the acoustic parameters that defined the vocalizations were studied. The response patterns shown by Arashiyama West group members, which were subject to a distinct change with only a slight difference of a single parameter, appeared to reflect strict underlying perceptual boundaries. This was analogous to the categorical perception that humans show with speech sounds. In contrast, continuous perception was exhibited by Arashiyama East group individuals. When several sounds were played back in combination to the former group, following stimuli were recognized by quite different cues from those by which the first sound was perceived. The groups' differences in vocal perception are discussed in terms of the ecological differences of the environments they inhabit.     

Changes In Rhesus Macaque 'Coo' Vocalizations during Early Development

In order to test whether ‘coo’ calls of young rhesus macaques, Macaca mulatta, undergo some modifications during early development, and to explore which factors may influence these changes, we studied the ontogeny of their contact call, the ‘coo’ call. Vocalizations were recorded during brief periods of social separation. Infants were either raised with their mothers and other conspecifics, or separated from their mothers at birth and housed in a nursery with other infants. We recorded calls uttered in the separation context from 20 infants. We digitized the first 50 calls of a given series and subjected them to a Fourier transform. From each frequency–time spectrum, we extracted 65 acoustic parameters using a software program (LMA 5.9). We then used a cluster analysis to separate the ‘coo’ calls from other call types. With increasing age, the ‘coos’ dropped in pitch and became more even. The course of amplitude became more constant and the call duration increased slightly. Nevertheless, we found a high intra‐individual variation throughout the 5 mo. Neither rearing condition nor sex had any apparent influence on age‐related changes in ‘coo’ structure. With one exception, all parameters that correlated with age could be explained by variation in weight. Therefore, we conclude that growth is the main factor accounting for the observed changes.     

Social Factors Influence the Acoustic Variability in the Long-distance Calls of Male Chimpanzees

Acoustic variability in the species-typical long-distance calls of male chimpanzees was investigated. Analysis of 13 acoustic features revealed that calls varied more within than between individuals. Although only a limited amount of acoustic variability was attributable to different populations, discriminant-function analysis confirmed that males from two populations produce acoustically distinguishable calls. Additional investigation suggested that social factors may contribute to the patterns of acoustic variation both between and within individuals. Matrix-permutation tests revealed a positive association between the amount of time males spent together and a measure of call similarity. Vocal similarities between individuals appeared to result from a dynamic process involving chorusing behaviour: males matched the acoustic characteristics of each other's vocalizations when calling together. Chorusing may also affect the degree of within-individual acoustic variation in calls. Males who chorused often with others produced more variable calls than individuals who chorused less often or called alone.     

Acoustical variations in sexually dimorphic features of distance calls in domesticated zebra finches (Taeniopygia guttata castanotis)

Species-specific distance calls (DCs) were recorded from Zebra finches (Taeniopygia guttata castanotis) obtained from three different breeding stocks: Japanese breeders that use Bengalese finches as fostering parents, and Japanese and American breeders that let natural parents rear Zebra finches. These calls were analyzed for five acoustic parameters that were shown to be sexually dimorphic in wild Zebra finches. Male Zebra finches had DCs that were variable among breeding stocks and among individuals. Female DCs recorded from Bengalese-fostered birds were generally longer in duration and higher in pitch than those recorded from Zebra-finch-reared birds, males and females in each breeding stock differed in at least one acoustic parameter, but that parameter was unique in each of the breeding stocks. These results suggest that although sexual dimorphism in Zebra finch DCs has gradually disappeared during the process of domestication, at least one acoustic attribute which allows discrimination between the calls of the sexes has been preserved.     

Species differences of male loud calls and their perception in sulawesi macaques

Playback experiments were conducted to investigate interspecific discrimination of male loud calls in Sulawesi macaques. Loud calls of four macaque species living in Sulawesi (Macaca tonkeana, M. maurus, M. hecki, andM. nigrescens) and a control stimulus (an 8-sec frequency modulated sound) were played back to semi-free-ranging Tonkean macaques (M. tonkeana). A preliminary acoustic analysis indicated that the calls of these four species differ in some spectral and temporal features. In the playback experiments, Tonkean macaques responded in a similar manner to conspecific calls and calls of two other species,M. maurus andM. hecki. In contrast, animals responded more weakly to the call ofM. nigrescens and the control stimulus. Males responded more strongly than females to all stimuli, while females appeared to be more discriminating for species differences than males. Analyses on the acoustic features of loud calls suggested that high frequency, wide frequency range, and repetition of sound units at a high rate elicit quick responses from animals.     

Intergroup encounters in wild moor macaques (<Emphasis Type="Italic">Macaca maurus</Emphasis>)

We studied intergroup encounters among moor macaques at the Karaenta Nature Reserve, South Sulawesi, Indonesia. Group B has been observed on the basis of individual identification since 1988. We analyzed 85 encounters between members of Group B and members of neighboring groups from September 1990 to November 1998. The average frequency of intergroup encounters was 0.035/hour. Neither the presence of females in estrus nor rainfall had an effect on encounter frequency. Behaviors of moor macaques during intergroup encounters differed from those of Japanese macaques. In moor macaques, no intergroup interactions with body contact were observed during encounters, and females never directed aggression toward members of different groups. The present study did not confirm the prediction of the model ofvan Schaik (1989). Extension of the existing models is required to explain the difference in female dominance styles among macaques by socioecological factors.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.