Age Differences in the Responses to Adult and Juvenile Alarm Calls by Bonnet Macaques (Macaca radiata)

This study examined the differential responses to alarm calls from juvenile and adult wild bonnet macaques ( Macaca radiata ) in two parks in southern India. Field studies of several mammalian species have reported that the alarm vocalizations of immature individuals are often treated by perceivers as less provocative than those of adults. This study documents such differences in response using field-recorded playbacks of juvenile and adult alarm vocalizations. To validate the use of playback vocalizations as proxies of natural calls, we compared the responses of bonnet macaques to playbacks of alarm vocalizations with responses engendered by natural alarm vocalizations. We found that the frequency of flight, latency to flee, and the frequency of scanning to vocalization playbacks and natural vocalizations were comparable, thus supporting the use of playbacks to compare the effects of adult and juvenile calls. Our results showed that adult alarm calls were more provocative than juvenile alarm calls, inducing greater frequencies of flight with faster reaction times. Conversely, juvenile alarm calls were more likely to engender scanning by adults, a result interpreted as reflecting the lack of reliability of juvenile calls. Finally, we found age differences in flight behavior to juvenile alarm calls and to playbacks of motorcycle engine sounds, with juveniles and subadults more likely to flee than adults after hearing such sounds. These findings might reflect an increased vulnerability to predators or a lack of experience in young bonnet macaques.     

Perceptual salience of acoustic differences between conspecific and allospecific vocalizations in African collared-doves

In speciation events, species-distinct vocal signals can diverge acoustically in many ways. Signal receivers have to be able to distinguish conspecific from allospecific vocalizations, and the perceptual salience of acoustic features is therefore expected to be an important factor in the evolution of such vocalizations. We tested how dissimilar the species-identifying perch-coos of 12 closely related turtle-dove species (genus Streptopelia) are, as perceived by one of its members, S. roseogrisea. With operant, psychoacoustic methods we trained six doves to respond only to their conspecific coo. Responses to the perch-coos of the 12 other dove species were used as a measure of their perceptual similarity to conspecific perch-coos. Turtle-doves differentiated between the allospecific coos: some were perceived as more similar to their own species' coo than others. With multiple regression analysis we identified three acoustic features that correlated with these differences in perceptual similarity: coo duration, minimum frequency and Wiener entropy. In contrast to findings in other bird species, duration was by far the most important feature in the discrimination between conspecific and allospecific vocalizations for S. roseogrisea. The results suggest that this is due not only to the coos of the various species differing in duration but also to a comparatively high perceptibility of the differences in duration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Comparing Contact Calling Between Black Tufted-Ear Marmosets (<Emphasis Type="Italic">Callithrix penicillata</Emphasis>) in a Noisy Urban Environment and in a Quiet Forest

All habitats have some level of noise but anthropogenic sounds such as those produced by traffic are structurally different from natural sounds, and could cause organisms living in noisy urban areas to modify their vocal communication. We compared temporal and spectral parameters of contact calls in black tufted-ear marmosets (Callithrix penicillata) living in a noisy and a quiet area. From February 2009 to March 2012 we recorded spontaneously produced phee vocalizations by marmosets in two areas in Minas Gerais, Brazil: a noisy urban park (N = 581) in Belo Horizonte, and a quiet natural forest, on Cauaia farm in Matozinhos city (N = 560). We measured the duration, frequencies, and rate of phee vocalizations. We found that marmosets’ phee vocalizations were significantly longer in the noisy area than in the quiet area. The low, high, and dominant frequencies were significantly lower in the noisy area than in the quiet area, and contact calling was less frequent in the noisy area than in the quiet area. We suggest that the differences between marmoset contact calls from noisy and quiet areas are influenced by anthropogenic noise.     

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.     

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.     

Analysis of acoustically evoked call suppression behaviour in a neotropical treefrog

We broadcast synthetic call notes to male Eleutherodactylus coqui treefrogs in their natural habitat. The frogs avoided acoustic overlap with relatively long duration tone stimuli by calling only within the short silent interval between tones. We also observed a temporal change in call pattern in response to tone stimuli of various frequencies and intensities. This response is the basis for construction of a behavioural auditory threshold function for this species. This function does not show a sensitivity maximum at frequencies corresponding to those in the advertisement call, and demonstrates that the frogs are capable of behaviourally responding to sounds over a frequency range which is greater than that required for detection of the species-specific vocalizations and sufficient for detection of at least one sympatric anuran species.     

Repeated decrease in vocal repertoire size in Streptopelia doves

Most bird species produce different acoustic signals in different behavioural contexts. This intraspecific variation in signal types is thought to be the result of selection for optimal communication in each context. Doves in the genus Streptopelia have three distinct behavioural contexts in which they produce coo vocalizations. Some Streptopelia species have three acoustically similar coo vocalizations associated with the three contexts, but in others the coo vocalizations differ in acoustic structure. Using a well-resolved phylogeny, we examined whether acoustic differentiation between coo types was the ancestral state. Unexpectedly, the results showed that the common ancestor of Streptopelia had differentiated coos rather than a single coo type. This result implies that context-specific acoustic signals disappeared from the vocal repertoire independently at least two times. We further tested whether different context-dependent signal types follow different evolutionary pathways and whether they differ in rate of evolutionary change. We found that the long-range signal (perch-coo) evolves at a higher rate than the short-range signal (bow-coo). These results are discussed in relation to selection for species recognition and transmission requirements.     

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.     

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.     

Experimental Evidence for Phonemic Contrasts in a Nonhuman Vocal System

The ability to generate new meaning by rearranging combinations of meaningless sounds is a fundamental component of language. Although animal vocalizations often comprise combinations of meaningless acoustic elements, evidence that rearranging such combinations generates functionally distinct meaning is lacking. Here, we provide evidence for this basic ability in calls of the chestnut-crowned babbler (Pomatostomus ruficeps), a highly cooperative bird of the Australian arid zone. Using acoustic analyses, natural observations, and a series of controlled playback experiments, we demonstrate that this species uses the same acoustic elements (A and B) in different arrangements (AB or BAB) to create two functionally distinct vocalizations. Specifically, the addition or omission of a contextually meaningless acoustic element at a single position generates a phoneme-like contrast that is sufficient to distinguish the meaning between the two calls. Our results indicate that the capacity to rearrange meaningless sounds in order to create new signals occurs outside of humans. We suggest that phonemic contrasts represent a rudimentary form of phoneme structure and a potential early step towards the generative phonemic system of human language.     

Imprinting on time-structured acoustic stimuli in ducklings

Filial imprinting is a dedicated learning process that lacks explicit reinforcement. The phenomenon itself is narrowly heritably canalized, but its content, the representation of the parental object, reflects the circumstances of the newborn. Imprinting has recently been shown to be even more subtle and complex than previously envisaged, since ducklings and chicks are now known to select and represent for later generalization abstract conceptual properties of the objects they perceive as neonates, including movement pattern, heterogeneity and inter-component relationships of same or different. Here, we investigate day-old Mallard (Anas platyrhynchos) ducklings’ bias towards imprinting on acoustic stimuli made from mallards’ vocalizations as opposed to white noise, whether they imprint on the temporal structure of brief acoustic stimuli of either kind, and whether they generalize timing information across the two sounds. Our data are consistent with a strong innate preference for natural sounds, but do not reliably establish sensitivity to temporal relations. This fits with the view that imprinting includes the establishment of representations of both primary percepts and selective abstract properties of their early perceptual input, meshing together genetically transmitted prior pre-dispositions with active selection and processing of the perceptual input.     

Detection and discrimination of natural calls in masking noise by birds: estimating the active space of a signal

We tested the ability of birds to detect and discriminate natural vocal signals in the presence of masking noise using operant conditioning. Masked thresholds were measured for budgerigars, Melopsittacus undulatus, and zebra finches, Taeniopygia guttata, on natural contact calls of budgerigars, zebra finches and canaries, Serinus canaria. Thresholds increased with increasing call bandwidth, the presence of amplitude modulation and high rates of frequency modulation in calls. As expected, detection thresholds increased monotonically with background noise level. Call detection thresholds varied with the spectral shape of noise. Vocal signals were masked predominantly by noise energy in the spectral region of the signals and not by energy at spectral regions remote from the signals. In all cases, thresholds for discrimination between calls of the same species were higher than thresholds for detection of those calls. Our data provide the first opportunity to estimate distances over which specific communication signals may be effective (i.e. their ‘active space’) using masked thresholds for the signals themselves. Our results suggest that measures of peak sound pressure level, combined with the spectrum level of noise within the frequency channel having the greatest signal power relative to background noise, give the most similar results for estimating a signal's maximum communication distance across a variety of sounds. We provide a simple model for estimating likely detection and discrimination distances for the signals tested here. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.     

Sex Differences in Infant Rhesus Macaque Separation–Rejection Vocalizations and Effects of Prenatal Androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation–rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Aggressive howling in wolves

During two studies that investigated the responses of wolf packs to either human simulations or pre-recorded playbacks of wolf, Canis lupus, howling, single adult wolves from five different packs approached my location and howled on a total of six occasions. The howls uttered by these close-approaching wolves were significnatly deeper in pitch than comparable samples of howls recorded from animals that did not approach. In addition, howls of two of the five animals differed in structure from most of the other howls recorded during both studies. These close-approach howls were characterized by the presence of harmonically unrelated frequency sidebands near the end of the howl. This feature was rate in howls recorded during occasions when wolves kept their distance. These results indicate that the structure of wolf howling during aggressive interactions with strange wolves follows Morton's (1977) motivation-structural rules, which state that natural selection will favour the use of low-frequency, harsh sounds by hostile animals. This relationship follows from the physical constraints of vocal production: animals of larger size can produce sounds of lower pitch and harsher tonal quality. As body size is a primary determinant in the outcome of aggressive interactions, vocalizations signalling size (i.e.low-pitched, harsh sounds) will be of selective value for individuals engaged in aggressive interactions.     

A statistical analysis of the social behavior of the male stumptail macaque (Macaca arctoides)

The social behavior of male stumptail macaques was analyzed in terms of behavioral sequences recorded during paired encounters in a large test cage. Recurrent patterns of behavioral sequences were sought and used to hypothesize the structure of motivational systems of social behavior as has been done previously for other species. In addition to traditional statistical analyses to determine which dyadic behavioral sequences were nonrandom, there were several methodological innovations. Instead of analyzing behavior as a single channel of communications, we analyzed three independent channels and considered their inter-correlations: 1) acts and postures; 2) vocalizations; and 3) facial expressions. Also, we analyzed not only within-animal behavioral sequences but between-animal sequences as well. Results were derived from 40 tests, most of which included vigorous agonistic and sexual interactions and a behavioral repertoire similar to that of adult male stumptail macaques observed by previous investigators. There were 30 acts and postures, eight facial expressions, and seven vocalizations that occurred more than five times. Many acts and postures occurred in nonrandom sequences, 43 such sequences within-animal and 40 between-animal. From these sequences and their correlations with specific vocalizations and facial expressions, it was possible to differentiate six categories of social behavior that may correspond to six different motivational systems: offense, defense, submission, groom and contact, male sexual behavior, and display. Both the frequency of behaviors in each category and the nature of the behavioral sequences were affected by the relative dominance of the two animals.     

Body Size Effects on the Acoustic Structure of Pigtail Macaque (Macaca nemestrina) Screams

Scream vocalizations produced by pigtail macaques during agonistic encounters were classified according to caller body weight (small, medium, large) on the basis of six frequency-related acoustic variables using direct discriminant analysis. Separate discriminant analyses were run for: 1. calls produced when the attack involved an opponent higher-ranking than the victim and contact occurred, and 2. calls produced when the opponent was higher-ranking, but no contact occurred. Screams were correctly classified as to the caller's weight class at levels significantly above those expected by chance alone. Screams given during contact aggression were classified significantly better than those given in the absence of contact. The effect of greater arousal level (fear) on the frequency range of calls may account for this difference. Macaque screams are representational signals that are important in the solicitation of agonistic aid from allies in the social group. That a relationship between body size and the frequency of screams is nonetheless evident argues for the fundamental nature of the relationship.     

Non‐Selective and Time‐Dependent Behavioural Responses of Common Toads (Bufo bufo) to Predator Acoustic Cues

Acoustic predator recognition has rarely been studied in anurans, in spite of the fact that hearing is widespread in these animals and that it has been demonstrated to play an important role in both arthropods and other vertebrates. Using field playback experiments, we tested the hypothesis that adult common toads (Bufo bufo) are capable of recognizing natural vocalizations of a common predator, the Eurasian otter (Lutra lutra), and show antipredator responses. We found that toads exposed to both natural (two types of otter sounds) and synthetic stimuli [white noise (WN) and otter sound‐based amplitude modulated WN] increased time allocated to locomotion and escape behaviour. These responses were correlated with time elapsed from sunset to the onset of testing and were independent from the type of acoustic signal, toad features and other environmental factors monitored. We conclude that B. bufo has not developed a selective recognition of predator vocalizations, suggesting that low‐frequency or seismic sounds associated with predator movements may provide anurans with better cues about an approaching risk. We propose that the time‐dependent response to acoustic stimuli of common toads represents a case of threat‐sensitivity and demonstrates that it can occur even when the response to the threat is not predator specific.     

Sex differences in infant rhesus macaque separation-rejection vocalizations and effects of prenatal androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation-rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Selective and Efficient Neural Coding of Communication Signals Depends on Early Acoustic and Social Environment

Previous research has shown that postnatal exposure to simple, synthetic sounds can affect the sound representation in the auditory cortex as reflected by changes in the tonotopic map or other relatively simple tuning properties, such as AM tuning. However, their functional implications for neural processing in the generation of ethologically-based perception remain unexplored. Here we examined the effects of noise-rearing and social isolation on the neural processing of communication sounds such as species-specific song, in the primary auditory cortex analog of adult zebra finches. Our electrophysiological recordings reveal that neural tuning to simple frequency-based synthetic sounds is initially established in all the laminae independent of patterned acoustic experience; however, we provide the first evidence that early exposure to patterned sound statistics, such as those found in native sounds, is required for the subsequent emergence of neural selectivity for complex vocalizations and for shaping neural spiking precision in superficial and deep cortical laminae, and for creating efficient neural representations of song and a less redundant ensemble code in all the laminae. Our study also provides the first causal evidence for ‘sparse coding’, such that when the statistics of the stimuli were changed during rearing, as in noise-rearing, that the sparse or optimal representation for species-specific vocalizations disappeared. Taken together, these results imply that a layer-specific differential development of the auditory cortex requires patterned acoustic input, and a specialized and robust sensory representation of complex communication sounds in the auditory cortex requires a rich acoustic and social environment.     

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.