Individual vocal differences of the coo call in Japanese monkeys

We investigated individual vocal characteristics of the coo call in Japanese monkeys. The goal of the study was to determine which parameters are individual discriminators (for individuals of different ages and sexes) and to test whether those differences were similar for individuals of same age and sex. A discriminant analysis realized on eight individuals pointed out that three parameters (call duration, start and end frequencies of the fundamental component) differentiated individuals efficiently and was validated by a second discriminant analysis realized on three same-age females.     

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.     

Spectrographic Description of Vocalizations in Captive Otolemur garnettii

To advance knowledge of the vocal communication associated with close proximity social interactions in Garnett's greater bush baby (Otolemur garnettii), we measured acoustic and temporal properties of vocalizations from videotaped recordings of captives in two main social contexts: mother-infant interactions and adult male-female pair introductions and reintroductions. We used a real-time sonagraph or software program to display, edit, and analyze vocal waveforms, and to provide wideband and narrowband spectrograms. Vocalization characteristics measured include fundamental frequency (via inspection of harmonics) and spectral features such as formant frequency, intensity, and duration. The vocal repertoire contained 4 major types of vocalizations: 1) barks and complex multiple bark sequences, 2) low frequency flutter/hums and growls, 3) high frequency clicks and spits, and 4) noisy shrieks. We describe several vocalizations for the first time and provide a clear classification of some of them on the basis of call durations (long/short growls). Complex bark sequences, previously described as distant communication calls, were invariant and were not often emitted by individuals when in close proximity. When classified spectrographically, the remaining 3 call types, which occurred when individuals were in close proximity, were less stereotypical, and gradations within call types were apparent. Our results show that although nocturnal and non-gregarious, complex communicatory signals of bush babies constitute a vocal repertoire formerly thought to be characteristic only of diurnal, gregarious primates.     

The first call note of the Anhui tree frog (Rhacophorus zhoukaiya) is acoustically suited for enabling individual recognition

The effective production of acoustic signals is critically important for intraspecific communication in vocal animals; however, it is also highly time-consuming, energetically demanding and likely to increase predation risks. Thus, we hypothesized that the biological significance of each component of complex acoustic signals would differ serving specific functions and that the first component of such signals would be most important for social signalling and exhibit unique acoustic characteristics because of the precedence effect. To test this hypothesis, we measured temporal and spectral acoustic parameters for each note in the advertisement calls of the Anhui tree frog (Rhacophorus zhoukaiya), a species in which males build mud burrows and call from within these nests. Multivariate analyses including hierarchical cluster analysis and multidimensional scaling were used, based on temporal and spectral acoustic parameters for each of 10 notes/call. These results show that the first call notes form one cluster while the other notes form a second cluster in multidimensional space when the parameters measured were normalized. Furthermore, the temporal and spectral sound attributes of the first call note provide sufficient information for discrimination between different individuals. Moreover, discriminant analysis showed that the fundamental frequency of the first note is sufficient to identify individuals when the data are not normalized. Taken together, these results indicate that the first call note is poised to play an important role in Anhui tree frog vocal communication insofar as the temporal and spectral features provide sufficient information for individual recognition.     

Discrimination of sinusoidally frequency-modulated sound signals mimicking species-specific communication calls in the FM-bat Phyllostomus discolor

In the lesser spear-nosed bat, Phyllostomus discolor, maternal directive calls are characterized by an individual type of sinusoidal frequency modulation (= SFM) pattern. Beside modulation frequency, modulation depth, carrier frequency, and number of modulation cycles per call contribute to the mother's vocal signature. Since juvenile P. discolor learn to adapt their isolation calls to the corresponding call characteristics of the own mother or even to playback of a computer-stored directive call, if hand-reared in the absence of conspecifics, the bats' auditory system ought to be able to resolve interindividual differences in communication call structure. However, quantitative psychoacoustic data on the discrimination of SFM signals in this species are not available. Thus, in the present study, lesser spear-nosed bats were trained in a two-alternative forced-choice procedure to discriminate between two alternatingly presented SFM sound signals differing in modulation frequency. Other characteristics of acoustic stimuli were identical and designed to mimick the fundamental of species-specific calls. By gradually reducing the difference in modulation frequency between both stimuli within the behavioural relevant range until the animals' performance dropped below the 75%-correct level, a considerable auditory spectro-temporal resolution has been revealed. Particularly in comparison to the overall interindividual variation of this call parameter (minimal modulation frequency = 49 Hz, maximum = 100 Hz), the determined average difference limen for modulation frequency of 2.42 ± 0.29 Hz seems substantial and sufficient for labelling individuals. Accepted: 30 November 1996     

Who is Calling? Intraspecific Call Variation in the Aromobatid Frog Allobates femoralis

Many territorial species respond less aggressively to familiar neighbours than to unfamiliar floating strangers based on individual differences in acoustic signals. This form of social recognition, termed neighbour–stranger discrimination (NSD) or dear-enemy phenomenon has been reported so far from three anuran species. To investigate the potential of auditory signal features to convey information on sender's identity, we determined patterns of within-male and between-male variability in the advertisement call of the aromobatid frog Allobates femoralis . We examined 285 calls from 19 males to assess those call properties showing sufficient and reliable inter-individual differences to function as possible recognition cues. Beside calls per call bout and call rate, all other examined call properties were more variable among males than within males. Generally, temporal call features showed higher between- and within-male variability ratios than spectral properties and contributed mostly to distinguish individual males in the discriminant-function analysis. Mean classification success of 64.9% correctly assigned calls to individual males is mainly attributable to three temporal call properties (duration of note 1 and 4, note repetition rate). Altogether, our results suggest that there is sufficient variation in the advertisement call to discriminate statistically among individual males. However, assessed call differences between A. femoralis males were rather small, suggesting that potential NSD might be based either on a combination of call features or even on the whole pattern of individual call variation instead on single call properties. Habituation–discrimination experiments in the field using modified playback signals to test for differential behavioural responses are required to confirm this hypothesis.     

Orangutan Long Call Degradation and Individuality Over Distance: A Playback Approach

Researchers have documented individual vocal recognition in several primate species but do not know whether the changes in acoustical parameters that might occur over distance influence the informational content of a call that relates to individuality. Accordingly, we performed playback experiments using male orangutan long-distance calls (long calls) and rerecorded them at increasing distances from the source. We aimed to determine 1) which acoustical parameters changed over distance and 2) whether the percentage of calls that a discriminant analyses would assign to the correct individual would change over distance. High-frequency harmonics were attenuated and lost with increasing distance, but other parameters did not change. The percentage of calls assigned to the correct individual did not change over distance, indicating that even though there are some acoustical changes over distance the opportunity for other individuals to recognize the caller remains similar until ≤300 m, which was the maximum distance at which we rerecorded calls. Extending similar experiments to other primate species and other taxa, while subsequently conducting experiments to assess whether individual discrimination by receivers is indeed based on relatively stable acoustical parameters, would forward our understanding of acoustic communication.     

Individually Specific Call Feature Is Not Used to Neighbour-Stranger Discrimination: The Corncrake Case

In various contexts, animals rely on acoustic signals to differentiate between conspecifics. Currently, studies examining vocal signatures use two main approaches. In the first approach, researchers search for acoustic characteristics that have the potential to be individual specific. This approach yields information on variation in signal parameters both within and between individuals and generates practical tools that can be used in population monitoring. In the second approach, playback experiments with natural calls are conducted to discern whether animals are capable of discriminating among the vocal signatures of different individuals. However, both approaches do not reveal the exact signal characteristics that are being used in the discrimination process. In this study, we tested whether an individual-specific call characteristic – namely the length of the intervals between successive maximal amplitude peaks within syllables (PPD) – is crucial in neighbour-stranger discrimination by males of the nocturnal and highly secretive bird species, the corncrake (Crex crex). We conducted paired playback experiments in which corncrakes (n = 47) were exposed to artificial calls with PPD characteristics of neighbour and stranger birds. These artificial calls differed only in PPD structure. The calls were broadcast from a speaker, and we recorded the birds'' behavioural responses. Although corncrakes have previously been experimentally shown to discriminate between neighbours and strangers, we found no difference in the responses to the artificial calls representing neighbours versus strangers. This finding demonstrates that even if vocal signatures are individual specific within a species, it does not automatically mean that said signatures are being crucial in discrimination among individuals. At the same time, the birds'' aggressive responses to the artificial calls indicated that the information transmitted by PPDs is important in species-specific call recognition and may be used by males and/or females to evaluate sender quality, similarly like sound frequency in some insect species.     

Vocal signature in capybara,Hydrochoerus hydrochaeris

Social groups of capybaras are stable and cohesive. The species’ vocal communication is complex and mediates social interaction. The click call is emitted in a variety of contexts by animals from all age groups, but differs among groups; its attributed function is to keep contact among animals. To evaluate the presence of individual characteristics in the click call of capybaras, we recorded the vocalizations emitted spontaneously by six adults kept either solitary or in groups. We selected and measured the acoustic parameters of 300 click call phrases, 50 per individual. The parameters were submitted to a discriminant function analysis that revealed a classification accuracy of 76.8 %. A General Linear Model analysis revealed significant differences among the six individuals, and post hoc results showed that differences between a given pair were different from those of any other pair. The acoustic parameters that most contributed to discriminate the individual calls were click interval duration and click duration, suggesting that temporal parameters are more important than frequency parameters for individuals’ discrimination. The findings of individual characteristics in the click calls indicate that these vocalizations can be used as vocal signatures during social interactions.     

A comparison of individual distinctiveness in three vocalizations of the dwarf mongoose (Helogale parvula)

Individual specificity can be found in the vocalizations of many avian and mammalian species. However, it is often difficult to determine whether these vocal cues to identity rise from “unselected” individual differences in vocal morphology or whether they have been accentuated by selection for the purposes of advertising caller identity. By comparing the level of acoustic individuality of different vocalizations within the repertoire of a single species, it is possible to ascertain whether selection for individual recognition has modified the vocal cues to identity in particular contexts. We used discriminant function analyses to determine the level of accuracy with which calls could be classified to the correct individual caller, for three dwarf mongoose (Helogale parvula) vocalizations: contact, snake, and isolation calls. These calls were similar in acoustic structure but divergent in context and function. We found that all three call types showed individual specificity but levels varied with call type (increasing from snake to contact to isolation call). The individual distinctiveness of each call type appeared to be directly related to the degree of benefit that signalers were likely to accrue from advertising their identity within that call context. We conclude that dwarf mongoose signalers have undergone selection to facilitate vocal individual recognition, particularly in relation to the species’ isolation call.     

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.     

Flexibility as a Strategy for Avoiding Call Overlap in Male Anhui Treefrogs

Male-male vocal competition is critical for mating success in anuran species; however, it remains unknown that how males regulate their competitive strategies dynamically during competition because calling is highly time-consuming, energetically demanding and likely to increase predation risks. Since different parts of calls will encode different information for vocal communication, we hypothesized that competitive strategies of male frogs may be modulated by the temporal and spectral features of different call notes. To test this hypothesis, the natural advertisement calls(OC), its modified versions with the first call note replaced by white noise(WN) or other notes and with the fifth call note replaced by WN, were played back to the Anhui tree frogs(Rhacophorus zhoukaiyae). Results showed that 1) males produced more competitive calls in response to acoustic stimuli compared to their baseline calling during silence; and 2) males emitted more non-overlapping calls compared to overlapping calls in response to the acoustic stimuli. These results are consistent with the idea that males are flexible to acoustic signals and their competition strategies are modulated dynamically by social contexts.     

Diversity of the Vocal Signals of Concave-Eared Torrent Frogs (Odorrana tormota): Evidence for Individual Signatures

Male concave-eared torrent frogs ( Odorrana tormota ) have an unusually large call repertoire and have been shown to communicate ultrasonically. We investigated the individual specificity of male advertisement calls in order to explore the acoustic bases of individual recognition, which was demonstrated in an accompanying study. Vocalizations of 15 marked males were recorded in the field. A quantitative analysis of the signals revealed eight basic call-types. Two of them (the single- and multi-note long-calls) were investigated in more detail. Long-calls were characterized by pronounced and varying frequency modulation patterns, and abundant occurrence of nonlinear phenomena (NLP), i.e., frequency jumps, subharmonics, biphonations and deterministic chaos. The occurrence of NLP was predictable from the contour of the fundamental frequency in the harmonic segment preceding the onset of the NLP, and this prediction showed individual-specific patterns. Fifteen acoustic variables of the long calls were measured, all of which were significantly different among individuals, except biphonic segment duration. Discriminant function analysis (DFA) showed that 54.6% of the calls could be correctly assigned to individual frogs. The correct classification was above chance level, suggesting that individual specificity of calls underlie the ability of males to behaviorally discriminate the vocal signals of their neighbors from those of strangers, a remarkable feat for a frog species with a diverse vocal repertoire. The DFA classification results were lower than those for other anurans, however. We hypothesize that there is a tradeoff between an increase in the fundamental frequency of vocalizations to avoid masking by low-frequency ambient background noise, and a decrease in individual-specific vocal tract information extractable from the signal.     

Responses of golden-backed uakaris, <Emphasis Type="Italic">Cacajao melanocephalus</Emphasis>, to call playback: implications for surveys in the flooded Igapó forest

We investigated the potential use of call playback for surveying the elusive golden-backed uakari (Cacajao melanocephalus), a diurnal social primate that typically inhabits the relatively inaccessible black-water swamp forests of the upper Amazon (Igapó forest) during the wet season. Furthermore, our objective was to understand better the functions of vocalisations of these rare and threatened monkeys. We focussed on the “tchó” call, a loud vocalisation that varies in temporal and frequency characteristics according to behavioural context and individual signaller (Bezerra et al. in Int J Primatol, 2010b). We investigated the vocal and behavioural responses of golden-backed uakaris from three Igapó areas to three different playback stimuli: own group calls (OGC); neighbouring group calls (NGC); and control (background noise). The call stimuli were used to simulate the unexpected presence of monkeys from the monkeys’ own and neighbouring Igapó areas. Playback of OGC and NGC increased calling and altered behaviour in golden-backed uakaris, whereas no noticeable response occurred to the control stimuli. Furthermore, there was no evidence of habituation to the call stimuli and the natural behavioural pattern of the groups was not obviously affected. Hence, call playback seems to be a valuable tool for locating these elusive monkeys in river surveys. Most of the agonistic-related behaviour observed after NGC playback was also observed after OGC playback. As golden-backed uakaris are not territorial, the presence of strange conspecifics to the area may not necessarily represent a more threatening situation. Our methods and results may also be useful for surveys of other primate species living in the Igapó forest and in other habitat types.     

No need to shout: Effect of signal loudness on sibling communication in barn owls Tyto alba

In animal communication, signal loudness is often ignored and seldom measured. We used a playback experiment to examine the role of vocal loudness (i.e., sound pressure level) in sibling to sibling communication of nestling barn owls Tyto alba. In this species, siblings vocally negotiate among each other for priority access to parental food resources. Call rate and call duration play key roles in this vocal communication system, with the most vocal nestlings deterring their siblings from competing for access to the food item next delivered by parents. Here, we broadcast calls at different loudness levels and call rate to live nestlings. The loudness of playback calls did not affect owlets' investment in call rate, call duration or call loudness. The rate at which playback calls were broadcast affected owlets' call rate but did not influence their response in terms of loudness. This suggests that selection for producing loud signals may be weak in this species, as loud calls may attract predators. Moreover, given that owlets do not overlap their calls and that they communicate to nearby siblings in the silence of the night, loud signals may not be necessary to convey reliable information about food need.     

Vocal Repertoire of Golden-backed Uakaris (<Emphasis Type="Italic">Cacajao melanocephalus</Emphasis>): Call Structure and Context

The study of vocal behavior can reveal important aspects of how and why a species communicates in relation to ecological and social challenges. We here focus on vocal communication in golden-backed uakaris (Cacajao melanocephalus), diurnal, pitheciine monkeys that exhibit fission-fusion social organization and typically inhabit dense forests that limit the potential for visual communication. Moreover, the species spends little time engaged in tactile or olfactory communication, e.g., social grooming and scent marking, respectively. Hence, vocalizations may be very important for the coordination of social organization in these monkeys. We 1) categorized golden-backed uakari vocalizations, 2) ascertained their behavioral context, and 3) investigated whether golden-backed uakari calls can encode information about the signaler. We observed the monkeys during 2 wet seasons in the flooded igapó forest of Jaú National Park, Brazil. We showed that golden-backed uakaris have 9 call types in their vocal repertoire, all distinguishable by ear and from analysis of spectrograms. Some calls, e.g., play-specific calls, were used only in particular behavioral contexts, and by individuals of specific age, whereas others were emitted under a range of situations. The structure of the loud tchó call varied among individuals, and according to behavioral context, i.e., whether individuals were foraging/feeding, traveling, or performing agonistic interactions. This knowledge of the species’ vocal repertoire is valuable for surveying the monkeys acoustically in habitats where visual surveys are difficult.     

Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques

To date, there have been no investigations of the behavioral effects of interleukin-1 (IL-1) in nonhuman primates. In this study the locomotor behavior and vocalizations of juvenile rhesus monkeys were monitored for 45 minutes following intravenous injections of recombinant human IL-1 alpha. In addition, their reaction to a broadcasted recording of infant monkey distress calls was determined 20 minutes after the beginning of each test session. IL-1 induced sleep-like inactivity and significantly diminished the monkey's behavioral and vocal responses to the broadcasted calls. The coo calls uttered by the monkeys following IL-1 treatment also had a longer duration and lower fundamental frequency than calls during the control condition. As several studies have indicated that behavioral effects of IL-1 may be mediated by corticotropin-releasing hormone (CRH), a second group of rhesus monkeys was given injections of CRH. CRH did not alter behavior or call structure at the dose administered. These results extend previous research on the behavioral effects of IL-1 to include the nonhuman primate and provide the first evidence that cytokines can affect vocal communication in rhesus monkeys. © 1995 Wiley-Liss, Inc.     

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.     

Is there variation in the response to contact call playbacks across the hybrid zone of the parrot Platycercus elegans?

Learned vocal signals could be important in the formation of prezygotic isolation between two hybridising taxa. This study examined whether vocal variation in the parrot Platycercus elegans facilitates the separation of individuals from two subspecies, P. e. elegans (CR) and P. e. flaveolus (YR). CR and YR have very different plumage coloration, respectively deep crimson and pale yellow, but hybridise where they meet creating an intermediate population (WS). In a factorial design playback experiment, we conducted 108 playback trials on three focal populations (YR, WS, CR), in and around this area of hybridisation, to test if they respond differently to contact calls from their own or another population. We also analysed whether differences in acoustic variables of the stimulus calls predicted the response to the call. We did not find any indication that individuals from the three focal populations responded differently to calls sampled from their own or another subspecies. We did find an effect of two of the five acoustic variables that we used to describe and classify contact calls from the three source populations. Specifically, duration of the stimulus call positively affected the response from individuals from WS and negatively the response from CR, and CR responded more to stimulus calls with a lower peak frequency. Overall, we found no indication that acoustic variation in contact calls on a subspecies level is involved in maintaining plumage colour differences between P. e. elegans and P. e. flaveolus subspecies.     

Evidence for Dialects in Three Captive Populations of Common Marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The vocal repertoires of nonhuman primates have long been thought to be invariable across populations and not to result from vocal learning. However, increasing evidence suggests that learning does influence vocal production in nonhuman primates, and that several species modify the structure of their calls in response to social or environmental influences. Vocal usage learning refers to the process whereby an individual learns in which circumstances to produce a certain call type, whereas vocal production learning refers to the process in which signals get modified as the result of individual experiences. Common marmosets (Callithrix jacchus) show socially mediated vocal plasticity as adults and during vocal development. This propensity to engage in simple forms of vocal production learning (accommodation) should produce population-level differences in call structure. To test this prediction, we compared the vocalizations of three captive populations of common marmosets. We analyzed the acoustic structure of 1337 phee calls, 461 trills, and 3611 food calls and compared them with a permutated discriminant function analysis. We found that all call types differed significantly between the three populations, and 76–98% of the calls were correctly classified. As physical differences in body mass and environmental differences between colonies could not explain the call differences, we conclude that vocal accommodation is the most likely explanation for the differences in call structure. This will allow us to further investigate the role and importance of vocal learning in a species increasingly used to study vocal learning and language evolution.