Antiphonal call timing in marmosets is behaviorally significant: interactive playback experiments

Studies of primate vocal communication systems have generally focused on vocalizations and the information they convey to conspecifics. But the vocalizations are not the only sources of information. Aspects of each species vocal behaviors are likely to be communicatively rich as well. During vocal interactions, for example, the latency delay between the calls could communicate an important message to the signal receiver, such as an interest and willingness to socialize. Here we employed novel, interactive playback software to address this issue in the antiphonal calling behavior of common marmosets. In these experiments, we parametrically varied the latency delay of antiphonal call stimuli and measured its effects on subjects’ resultant vocal behavior. Results showed that marmosets produced successively fewer antiphonal call responses during test conditions with increasing latency delays. Moreover, although subjects produced significantly more antiphonal than spontaneous calls in conditions with antiphonal call timing delays up to 9 s, a longer delay resulted in a significant decline in calling. These data suggest that antiphonal call timing is a salient cue for maintaining antiphonal calling interactions and may be used by marmosets to determine whether a subsequent call is produced in response to or independently of their own.     

Effects of proximity and behavioral context on acoustic variation in the coo calls of Japanese macaques

Acoustic features of coo calls in Japanese macaques (Macaca fuscata) show large and graded variation. To explore the relevance of acoustic variation in coo calls, I examined whether acoustic features differed by the caller's activity and proximity to group members. The subjects were five adult females from a wild, habituated group of Japanese macaques consisting of 23 individuals. Coo calls from the five females were recorded with their activity and proximity to group members. Acoustic features of 280 calls were measured with a sound spectrograph. Some of the acoustic variables differed by proximity but not by activity. The callers produced coo calls with larger frequency modulation and longer duration when they were far from group members compared to when they were near another member. The results suggest that Japanese macaques produce calls with more detectable and locatable features depending on the proximity to group members.     

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.     

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.     

Vocal communication of wild bonnet macaques (Macaca radiata)

Field observations and spectrographic analyses of sound recordings of South Indian bonnet macaques revealed a vocal repertoire of at least 25 basic patterns. The repertoire consists of well separated sound classes and acoustic categories connected by structural intergradation. Besides structural variations within and between different elements of the repertoire, the vocal system ofMacaca radiata is characterized by regular combinations of particular basic patterns. These combinations occurred not only between calls of similar structure and function but also between calls usually emitted in entirely different social contexts. According to the qualitative analysis, sex-specific asymmetries of the vocal behaviour were less pronounced than age-dependent characteristics. The comparison of clear call vocalizations ofMacaca radiata andM. fuscata revealed significant species-specific differences on the structural and the behavioural level. Evaluations of the structural features of alarm calls of various macaque species imply marked differences between members of thefascicularis group andsinica group on one hand and thesilenus group andarctoides group on the other.     

Threat calls in alliance formation by members of a captive group of Japanese monkeys

The vocal behavior of threat calls was investigated in a captive group of Japanese monkeys (Macaca fuscata fuscata). The vocalizations were heard most often when they undertook winner-support during triadic agonistic interactions. The likelihood of call emission in support of the winner was affected by the attributes of the participants, and not by the types of agonistic behavior. The calls were emitted by intermediate ranking animals frequently in support of high ranking animals and in support of females. The calling behavior of winner-supporters appears to advertise the partner and distant group members of their support for reciprocation in the near future.     

非线性鸣声对雄性凹耳蛙应答的影响

为了解非线性鸣声对凹耳蛙(Odorrana tormota)应答音的影响以及非线性鸣声是否能够增强鸣声的不可预测性,本研究通过回放非线性鸣声和线性鸣声来刺激陌生雄性凹耳蛙,并记录应答次数及统计分析应答音相关参数。结果表明,回放非线性鸣声时会引起陌生蛙(n=22)更多次数的应答,但两种刺激引起的首次应答时间没有显著差异。对应答音相关参数分析表明,线性鸣声引起的应答音在总时长上比非线性鸣声引起的应答音更长且具有显著差异,而其他声音参数(包括平均基频、最大基频、最小基频、主频)均没有显著差异。推测当陌生雄蛙听到同类鸣叫时,出于保护领地和资源的本能反应,陌生蛙都会第一时间作出反应,因此在两类声音的应答反应时间上并没有区别。而在应答次数上,非线性鸣声引起了凹耳蛙更多次数的应答,可能是由于鸣声中的非线性现象使得声音更加复杂,包含更多信息,容易提高声音接收者对这类声音的关注度。本研究结果表明,凹耳蛙鸣声中包含的非线性现象能够增强其声音的不可预测性,引起陌生蛙产生更多的应答次数。     

Behavioural response evoked by conspecific distress calls in two neotropical treefrogs

Anurans emit distress calls when attacked by predators as a defensive mechanism. As distress calls may trigger antipredator behaviour even in individuals that are not under attack, we tested whether this defensive behaviour induced behavioural changes in neighbouring conspecifics. We compared the behavioural responses of two species of Neotropical hylid frogs (genus Boana) to conspecific distress calls and white noise. Individuals of both species interrupted their vocal activity and decreased call rate after hearing the distress call. Natural variation on signal intensity calibrated among the nearest neighbours did not influence the response and we did not observe negative phonotaxis after any acoustic stimulus. Despite the fact that many predators are acoustically oriented, we could not determine if such response (reduced call rate) was induced by risk assessment or by the masking effect on advertisement calls. Boana faber responded similarly to white noise and distress calls, while B. bischoffi responded more intensely to distress calls. Duration of silence after playbacks in B. faber was longer than B. bischoffi. We suggest that, if the signals are interpreted as a risk cue by neighbouring conspecifics, each species may be preyed upon by different predators, as they may have led to distinct defensive strategies and different responses to distress calls. If risk assessment information is included in distress calls, it triggers behavioural responses only in the nearest neighbours, as we did not observe responses on the vocal activity of the interspecific chorus. Our results add relevant data about acoustic communication and interpretations by anurans, highlighting the importance of considering cues within common and widespread signals.     

Primate phonation: Anterior cingulate lesion effects on response rate and acoustical structure

Four juvenile rhesus monkeys (Macaca mulatta) that were conditioned to emit a discriminative vocal response underwent unilateral and bilateral lesions of anterior cingulate gyrus in stepwise sequence. Pre- and post-lesion measures of vocal response rate and acoustical features (call duration, amplitude, and fundamental frequency) were obtained for the conditioned task and for vocalization in the home colony (spontaneous vocalization). Unilateral lesions produced little consistent change in spontaneous “coo” vocalization rate and call duration. Conditioned vocalization of the monkeys exhibited no significant change in rate at this stage, although call duration was reduced significantly. Bilateral lesions produced no further modifications in acoustic properties of spontaneous calls, while the vocal rate decreased slightly. Conditioned calls were not significantly altered in acoustic features at this stage, although the discriminative vocalization rate was significantly decreased for all monkeys. The results indicate limited control over vocal motor systems by anterior cingulate cortex, while suggesting that this region participates in initiation of voluntary phonation.     

Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

Studies on primate vocalisation have revealed different types of alarm call systems ranging from graded signals based on response urgency to functionally referential alarm calls that elicit predator‐specific reactions. In addition, alarm call systems that include both highly specific and other more unspecific calls have been reported. There has been consistent discussion on the possible factors leading to the evolution of different alarm call systems, among which is the need of qualitatively different escape strategies. We studied the alarm calls of free‐ranging saddleback and moustached tamarins (Saguinus fuscicollis and Saguinus mystax) in northeast Peru. Both species have predator‐specific alarm calls and show specific non‐vocal reactions. In response to aerial predators, they look upwards and quickly move downwards, while in response to terrestrial predators, they look downwards and sometimes approach the predator. We conducted playback experiments to test if the predator‐specific reactions could be elicited in the absence of the predator by the tamarins’ alarm calls alone. We found that in response to aerial alarm call playbacks the subjects looked significantly longer upwards, and in response to terrestrial alarm call playbacks they looked significantly longer downwards. Thus, the tamarins reacted as if external referents, i.e. information about the predator type or the appropriate reaction, were encoded in the acoustic features of the calls. In addition, we found no differences in the responses of S. fuscicollis and S. mystax whether the alarm call stimulus was produced by a conspecific or a heterospecific caller. Furthermore, it seems that S. fuscicollis terrestrial alarm calls were less specific than either S. mystax terrestrial predator alarms or either species’ aerial predator alarms, but because of the small sample size it is difficult to draw a final conclusion.     

Subharmonics increase the auditory impact of female koala rejection calls

Although non‐linear phenomena are common in human and non‐human animal vocalisations, their functional relevance remains poorly understood. One theory posits that non‐linear phenomena generate unpredictability in vocalisations, which increases the auditory impact of vocal signals, and makes animals less likely to habituate to call repetition. Female koalas (Phascolarctos cinereus) produce vocal signals when they reject male copulation attempts that contain relatively high levels of non‐linear phenomena, and thus may function as attention grabbing vocal signals during the breeding season. To test this hypothesis, we used playback experiments: firstly, to determine whether female rejection calls induce heightened behavioural responses in free‐ranging male koalas during the breeding season, and secondly, to examine how the relative amount of non‐linear phenomena in rejection calls influences male behavioural response. The results show that male koalas look for longer towards speakers broadcasting playback sequences of male bellows followed by a series of female rejection calls than those broadcasting only male bellows. In addition, female rejection call sequences with more subharmonics, higher harmonics‐to‐noise ratios, and less biphonation produced the greatest male looking responses. Our findings support the hypothesis that female koala rejection calls function to grab male attention during the breeding season, and indicate that subharmonics are the main acoustic feature that increases the auditory impact of these vocal signals.     

Individual and Contextual Variation in Thomas Langur Male Loud Calls

Individual and contextual differences in male loud calls of wild Thomas langurs (Presbytis thomasi) were studied in northern Sumatra, Indonesia. Loud calls were given in the following contexts: morning calls, vocal responses to other groups, between‐group encounter calls and alarm calls. Loud call spectrograms were analysed for a large number of variables. With discriminant analyses, 14 variables were found to be important in distinguishing individuals and contexts. Loud calls were assigned to the correct individual in 95.6% of the cases (91.8% with ‘leave‐one‐out’ validation) and to the correct context in 52.2% of the cases (39.0% with ‘leave‐one‐out’ validation). Further analyses with two‐way anova s showed significant differences in both temporal and frequency variables between individuals and contexts. Loud calls seemed to differ between the contexts in functionally meaningful ways, relating to the distance of the intended receivers and to the urgency of the message. Observation showed that females in the caller's group collected infants more often in the between‐group encounter context and in the alarm call context than in the vocal exchange context. These differential responses suggest that the monkeys also perceive the measurable differences in loud call characteristics between the various contexts.     

The study of vocal communication of wild mandrills in Cameroon in relation to their social structure

The vocal repertoire of the mandrill (Mandrillus sphinx), a forest living baboon, is described, and their vocal communication analyzed quantitatively. Although the vocal repertoire of mandrills corresponds well to that of savanna living baboons,Papio, some characteristics differed, such as the development of long-distance calls and differentiation of vocalizations between age-sex classes. Vocal communication within a group was closely related to changes in the spatial distribution of group members, and the two most common vocalizations, crowing and 2PG, appear to function as contact calls. Based on the wide dispersion of food trees, a group of mandrills divided into several feeding groups (subgroups). The two types of contact call were given in different and in some senses complementary contexts, and helped to facilitate and maintain group integration. According to their acoustic structure, these calls are long distance calls. Influenced by the high-level of attenuation of vocalization on the forest floor, the mandrill has developed them as contact calls, instead of using the contact “grunt,” which is common to the savanna living baboons. Comparing the patterns of vocal exchanges of mandrills with those of gelada and hamadryas baboons which have a multi-levelled society, the social structure of the mandrill is discussed. From the analysis of the spatial distribution of vocal emission, a number of clusters of vocalizations were obtained. These clusters correspond to subgroups. The frequent female-female and female-male vocal exchange between subgroups of mandrills suggest that the relationships between subgroups are less closed than between the one-male units of gelada and hamadryas baboons. Furthermore some of these clusters include more than two vocalizing adult males, while in other clusters there are no vocalizing adult males. Thus, the social structure of mandrills is suggested to be multi-male rather than a multilevelled type. The absence of contact calls specific for short distance and the functional replacement of the grunting of all group members by persistent emission of a loud call (2PG) by usually just one adult male suggests that the social structure of mandrills is not exactly equivalent to that of the multimale troop of savanna living baboons. Usually the use of 2PG is monopolized by one adult male travelling in the rear part of the group. Such monopolization of 2PG emission and the pattern of 2PG-2PG or 2PG-roar exchanges by adult males in some cases indicate the existence of strong dominance relationships among adult males, and especially the existence of a leader male within a multi-male group of mandrills.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

Independence of Evoked Vocal Responses from Stimulus Direction in Burrowing Frogs Eupsophus (Leptodactylidae)

Localization of a sound source is important for animals in mating contexts: females generally orient towards signalling males, and males can estimate the position and quality of potential rivals. In anurans, the effect of sound direction on evoked vocal responses has been studied in males of Rana catesbeiana, which alter their vocal responses depending on the location of the stimulus. The current study explored the effects of sound direction in Eupsophus calcaratus, a frog that calls from inside burrows having resonance that would hinder the localization of incoming sounds. The vocal responses of 11 males to synthetic imitations of the conspecific advertisement call broadcast from loudspeakers positioned in front, to the right and left from the burrow openings were similar in terms of call rate, duration and latency. The invariance of the vocal responses indicates that for burrowing male frogs engaged in chorusing behaviour, the specific location of an opponent does not alter the persistence of vocal activity.     

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.     

Efficiency and Significance of Multiple Vocal Signals in Sibling Competition

Animals can compete for resources by displaying various acoustic signals that may differentially affect the outcome of competition. We propose the hypothesis that the most efficient signal to deter opponents should be the one that most honestly reveals motivation to compete. We tested this hypothesis in the barn owl (Tyto alba) in which nestlings produce more calls of longer duration than siblings to compete for priority access to the indivisible prey item their parents will deliver next. Because nestlings increase call rate to a larger extent than call duration when they become hungrier, call rate would signal more accurately hunger level. This leads us to propose three predictions. First, a high number of calls should be more efficient in deterring siblings to compete than long calls. Second, the rate at which an individual calls should be more sensitive to variation in the intensity of the sibling vocal competition than the duration of its calls. Third, call rate should influence competitors’ vocalization for a longer period of time than call duration. To test these three predictions we performed playback experiments by broadcasting to singleton nestlings calls of varying durations and at different rates. According to the first prediction, singleton nestlings became less vocal to a larger extent when we broadcasted more calls compared to longer calls. In line with the second prediction, nestlings reduced vocalization rate to a larger extent than call duration when we broadcasted more or longer calls. Finally, call rate had a longer influence on opponent’s vocal behavior than call duration. Young animals thus actively and differentially use multiple signaling components to compete with their siblings over parental resources.     

Monotony and the Information Content of Richardson's Ground Squirrel (Spermophilus richardsonii) Repeated calls: Tonic Communication or Signal Certainty?

The repetition of elements within an alarm signal is commonly thought to ensure that receivers have detected that signal, or to promote residual vigilance in light of the dangerous circumstances prompting the signal's initial production (tonic communication). Beyond alerting others and maintaining that state of alertness, however, repetitive signal elements may be parsed so as to encode information about the nature of potential threats. To determine how call length and variation in intersyllable latency might prove informative in the repetitive alarm vocalizations of Richardson's ground squirrels (Spermophilus richardsonii), we conducted a field‐based playback experiment quantifying antipredator responses to manipulated alarm calls. Free‐living juvenile squirrels were exposed to playbacks of 12 syllable (long) and six syllable (short) calls with a constant (monotonous) or changing (variable) call rate. The length of calls had no significant effect on the behaviour of call recipients during and immediately after call production; however, call recipients showed greater vigilance after the playback of monotonous calls than after variable calls. The absence of a call length effect is not consistent with tonic communication in the strict sense; rather, enhanced responsiveness to monotonous relative to variable calls suggests that multiple syllables, and the emergent patterns of intersyllable latency, communicate information about response urgency or the distance to a predatory threat. Only monotonous calls convey those aspects with any certainty on the part of the signaller and hence are selectively attended to by receivers.     

Experimental study of alarm calls of the oriental tit (Parus minor) toward different predators and reactions they induce in nestlings

Anti-predatory strategies of birds are diverse and may include predator-specific alarm calls. For example, oriental tit (Parus minor) parents can distinguish snakes from other predators and produce snake-specific referential vocalizations ("jar" call) when a snake poses a threat to their nest. The “jar” call has a very specific function to induce fledging of nestlings close to fledging age. This reaction ensures nestlings' survival in natural encounters with snakes that are capable of entering nest cavities and kill entire broods. Sciurid rodents, like chipmunks, may pose a similar threat to cavity-nesting birds. We explored the hypothesis that parents use the fledging-inducing alarm vocalizations in this situation, because chipmunks, like snakes, can kill the brood upon entering the nest cavity. We compared alarm calls of parents toward two predators (chipmunk and snake) who pose a similar threat to the nestlings in a nest cavity, and toward an avian predator (Eurasian jay) who cannot enter nest cavities and poses no threat to the nestlings in a nest. Our results show that the vocal responses of oriental tits were different among the three predators. This suggests that the acoustic properties of vocal responses to predators are different between predators of a similar hunting strategy (nest-cavity entering). The playback of recorded vocal responses of parents to chipmunks did not trigger the fledging of old nestlings, whereas the vocalizations toward a snake did, as shown by earlier studies. Our study suggests that the vocal response of parents does not carry information about the ability of predators to enter the nest cavity and confirms the special status of alarm calls triggered by snakes.