Hiroki Koda

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. Am. J. Primatol. 70:1055–1063, 2008.

Possible role of mother-daughter vocal interactions on the development of species-specific song in gibbons.

Mother-infant vocal interactions play a crucial role in the development of human language. However, comparatively little is known about the maternal role during vocal development in nonhuman primates. Here, we report the first evidence of mother-daughter vocal interactions contributing to vocal development in gibbons, a singing and monogamous ape species. Gibbons are well known for their species-specific duets sung between mates, yet little is known about the role of intergenerational duets in gibbon song development. We observed singing interactions between free-ranging mothers and their sub-adult daughters prior to emigration. Daughters sang simultaneously with their mothers at different rates. First, we observed significant acoustic variation between daughters. Co-singing rates between mother and daughter were negatively correlated with the temporal precision of the song’s synchronization. In addition, songs of daughters who co-sang less with their mothers were acoustically more similar to the maternal song than any other adult female’s song. All variables have been reported to be influenced by social relationships of pairs. Therefore those correlations would be mediated by mother-daughter social relationship, which would be modifiable in daughter’s development. Here we hypothesized that daughters who co-sing less often, well-synchronize, and converge acoustically with the maternal acoustic pattern would be at a more advanced stage of social independence in sub-adult females prior to emigration. Second, we observed acoustic matching between mothers and daughters when co-singing, suggesting short-term vocal flexibility. Third, we found that mothers adjusted songs to a more stereotyped pattern when co-singing than when singing alone. This vocal adjustment was stronger for mothers with daughters who co-sang less. These results indicate the presence of socially mediated vocal flexibility in gibbon sub-adults and adults, and that mother-daughter co-singing interactions may enhance vocal development. More comparative work, notably longitudinal and experimental, is now needed to clarify maternal roles during song development.

Flexibility and context-sensitivity during the vocal exchange of COO calls in wild Japanese macaques (Macaca fuscata Yakui)

This study investigated the extent to which vocal production in wild Japanese macaques, Macaca fuscata yakui, is flexible. Japanese macaques frequently exchange coo calls with other group members to maintain auditory contact. When a coo call is emitted but no other members respond within a short interval, the same monkey often emits another call repeatedly. This study focused on these two successive coo call sequences. First, the sequences of eleven females in a free-ranging group were recorded and analyzed. Comparisons of the acoustic properties between the initial and repeated coo calls revealed that the repeated call was higher in fundamental frequency and longer in duration than the initial call. Next, playback experiments were conducted to examine the efficiency of the exaggerated acoustic features of these repeated coo calls. Eight pairs of initial and repeated coo calls were prepared from eight female monkeys as the playback stimuli, and played back to the eight subject females. Comparisons of subject responses to the initial and repeated coo call stimuli revealed that the repeated call stimuli elicited more frequent vocal responses. These field observation and playback results suggest that monkeys might be able to modify the acoustic properties of vocalizations according to the preceding context so as to elicit a more effective vocal response from other group members. The pattern of vocal interactions among wild Japanese macaques is therefore likely to be flexible and to some extent context-sensitive.

Experimental evidence for the volitional control of vocal production in an immature gibbon

Volitional control of vocal production is an essential ability for vocal usage learning in animal calls. Operant conditioning of vocal production is one of the most direct experimental approaches for assessing volitional vocal control in animals. In this case study, we attempted operant conditioning of the vocalizations of an immature female white-handed gibbon ( Hylobates lar ). For the operant conditioning of vocal production, the gibbon was required to immediately vocalize in response to a V-sign cue by the human experimenters hand. During the 2-month period of intensive training for conditioning, the gibbon successfully learned to produce the contingent response of vocalizations. We again tested the conditioning with a 30-day interval after the completion of conditioning and were able to immediately show memorization of vocal conditioning. These results directly suggest greater volitional control of vocal production in gibbons than previously considered. Our study implies the possibility of upper level volitional control in this species, which involves differentiation of several call types in response to specific arbitrary stimuli over the motivational state.

Free-Ranging Macaque Mothers Exaggerate Tool-Using Behavior when Observed by Offspring

The population-level use of tools has been reported in various animals. Nonetheless, how tool use might spread throughout a population is still an open question. In order to answer that, we observed the behavior of inserting human hair or human-hair-like material between their teeth as if they were using dental floss in a group of long-tailed macaques (Macaca fascicularis) in Thailand. The observation was undertaken by video-recording the tool-use of 7 adult females who were rearing 1-year-old infants, using the focal-animal-sampling method. When the data recorded were analyzed separately according to the presence/absence of the infant of the target animal in the target animals proximity, the pattern of the tool-using action of long-tailed adult female macaques under our observation changed in the presence of the infant as compared with that in the absence of the infant so that the stream of tool-using action was punctuated by more pauses, repeated more often, and performed for a longer period during each bout in the presence of the infant. We interpret this as evidence for the possibility that they exaggerate their action in tool-using so as to facilitate the learning of the action by their own infants.

Age- and sex-dependent contact call usage in Japanese macaques

The question of the flexibility of nonhuman primate vocal communication remains open today, especially due to early evidence of innately guided vocal production. However, socially determined flexibility can be found when the debate is moved from vocal structure to vocal usage. While increasing evidence shows that the audience quality influences the vocal behaviour of nonhuman primates, the impact of the caller’s characteristics has been far less studied. Here, we tested the influence of an individual’s sex and age on the usage style of contact calls. We recorded contact calls of male and female Japanese macaques and compared the vocal usage styles of approximately 1-year-old juveniles with those of adults at various ages. We found, first, important differences in call usage style between juveniles and adults, the latter forming temporally ruled vocal exchanges respecting an interindividual turntaking principle. Moreover, sex differences were substantial in adults but nonexistent in juveniles. Finally, age continued to influence female vocal behaviour during adulthood, whereas dominance rank explained differences between adult males. Two nonexclusive mechanisms can explain this phenomenon, that is, a socially guided development of the appropriate form of calling versus an emotional maturation to control call emission, opening new lines of research on nonhuman primate vocal development of appropriate usages.

Japanese monkeys (Macaca fuscata) quickly detect snakes but not spiders: Evolutionary origins of fear-relevant animals.

Humans quickly detect the presence of evolutionary threats through visual perception. Many theorists have considered humans to be predisposed to respond to both snakes and spiders as evolutionarily fear-relevant stimuli. Evidence supports that human adults, children, and snake-naive monkeys all detect pictures of snakes among pictures of flowers more quickly than vice versa, but recent neurophysiological and behavioral studies suggest that spiders may, in fact, be processed similarly to nonthreat animals. The evidence of quick detection and rapid fear learning by primates is limited to snakes, and no such evidence exists for spiders, suggesting qualitative differences between fear of snakes and fear of spiders. Here, we show that snake-naive Japanese monkeys detect a single snake picture among 8 nonthreat animal pictures (koala) more quickly than vice versa; however, no such difference in detection was observed between spiders and pleasant animals. These robust differences between snakes and spiders are the most convincing evidence that the primate visual system is predisposed to pay attention to snakes but not spiders. These findings suggest that attentional bias toward snakes has an evolutionary basis but that bias toward spiders is more due to top-down, conceptually driven effects of emotion on attention capture. (PsycINFO Database Record

Influence of sound specificity and familiarity on Japanese macaques' (Macaca fuscata) auditory laterality.

Despite attempts to generalise the left hemisphere-speech association of humans to animal communication, the debate remains open. More studies on primates are needed to explore the potential effects of sound specificity and familiarity. Familiar and non-familiar nonhuman primate contact calls, bird calls and non-biological sounds were broadcast to Japanese macaques. Macaques turned their heads preferentially towards the left (right hemisphere) when hearing conspecific or familiar primates supporting hemispheric specialisation. Our results support the role of experience in brain organisation and the importance of social factors to understand laterality evolution.

Visual recognition of age class and preference for infantile features: implications for species-specific vs universal cognitive traits in primates.

Despite not knowing the exact age of individuals, humans can estimate their rough age using age-related physical features. Nonhuman primates show some age-related physical features; however, the cognitive traits underlying their recognition of age class have not been revealed. Here, we tested the ability of two species of Old World monkey, Japanese macaques (JM) and Campbells monkeys (CM), to spontaneously discriminate age classes using visual paired comparison (VPC) tasks based on the two distinct categories of infant and adult images. First, VPCs were conducted in JM subjects using conspecific JM stimuli. When analyzing the side of the first look, JM subjects significantly looked more often at novel images. Based on analyses of total looking durations, JM subjects looked at a novel infant image longer than they looked at a familiar adult image, suggesting the ability to spontaneously discriminate between the two age classes and a preference for infant over adult images. Next, VPCs were tested in CM subjects using heterospecific JM stimuli. CM subjects showed no difference in the side of their first look, but looked at infant JM images longer than they looked at adult images; the fact that CMs were totally naïve to JMs suggested that the attractiveness of infant images transcends species differences. This is the first report of visual age class recognition and a preference for infant over adult images in nonhuman primates. Our results suggest not only species-specific processing for age class recognition but also the evolutionary origins of the instinctive human perception of baby cuteness schema, proposed by the ethologist Konrad Lorenz.

Immature male gibbons produce female-specific songs

Abstract Gibbons are apes that are well known to produce characteristic species-specific loud calls, referred to as “songs.” Of particular interest is the sex specificity of the “great calls” heard in gibbon songs. However, little is known about the development of such calls. While great calls are given by female gibbons of various ages, they have never been recorded from males. Here, we report two observations of immature male gibbons from two different species, wild Hylobates agilis and captive H. lar, which spontaneously sang female-specific great calls. Based on the video clips, we conclude that immature males also have the potential to produce great calls. Our observations led us to propose a new hypothesis for the development of sexual differentiation in the songs of gibbons, and its implications for the general issue of sex-specific behavior in primates.