Age- and sex-specific patterns of vocal behavior in De Brazza's monkeys (Cercopithecus neglectus)

Although vocal production is strongly genetically determined in nonhuman primates, vocal usage is more likely to be influenced by experience. Nonetheless, sex differences in both production and usage can be found in the vocal repertoire of adults, but little attention has been paid to their ontogeny. Here, we provide the first comprehensive analysis of the vocal repertoire of De Brazza's monkeys (Cercopithecus neglectus), with particular attention to age- and sex-specific patterns. This species has special interest because it is the only monogamous species of guenons, but it nevertheless shares the strong sexual morphological and behavioral dimorphism seen in other guenons. A structurally based classification of calls recorded in 23 captive individuals has been cross-validated by an analysis of the associated contexts of emission. We identified sound units that could be uttered alone or concatenated to form 10 call types, including only three types shared by all age-sex-classes. Both age- and sex-discrepancy in terms of phonation could be explained by maturational changes and morphological dimorphism. In general, call production and usage parallel those seen in other guenons, suggesting that phylogeny and sexual dimorphism play important roles in vocal communication in this species. However, the boundary between adult male and female vocal repertoires appeared to be less strict than previously reported, suggesting that both sexes have the capacity to produce calls of the other sex but that social roles may constrain this expression. Similarly, age-specific vocal patterns would reflect respective social roles, and experience to some extent. Finally, calling rates would reflect age-/sex-specific degree of involvement in intragroup social networks. These findings highlight the relative importance of phylogeny, morphology, and social system on the shaping of individual repertoires in nonhuman primates.     

Vocal repertoire of cooperatively breeding Smooth‐billed Anis

Calls are functionally diverse signals that mediate behavior in a wide variety of contexts in both passerines and non‐passerines. However, the call‐based acoustic communication systems of non‐passerines have received less attention from investigators than those of passerines. We examined the vocal repertoire of Smooth‐billed Anis (Crotophaga ani), cooperatively breeding cuckoos that live in groups with multiple breeding pairs. We recorded calls from 22 groups over two breeding seasons at the Cabo Rojo National Wildlife Refuge in Puerto Rico. We identified 11 call types and one group vocalization, and used an automated sound measurement program to quantify their acoustic features. Discriminant function analysis (DFA) correctly classified 74.2% of calls based on these features. The vocal repertoire of Smooth‐billed Anis is larger than that reported for the three other species in the subfamily Crotophaginae. Smooth‐billed Anis have at least two alarm calls, two nest‐specific calls, and one nest defense call. We also identified one possible signal of aggressive intent, one possible appeasement signal, and two calls that may communicate identity. The relatively large vocal repertoire of Smooth‐billed Anis and association of distinct call types with different functions and contexts supports the main prediction of the social complexity hypothesis, i.e., species with more complex social systems will have more complex communication systems.     

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.     

Vocal behavior of Great Curassows,a vulnerable Neotropical bird

ABSTRACT The Cracidae rank among the most threatened families of Neotropical birds, and studies of their vocal behavior may help guide conservation and monitoring efforts. We describe the vocal behavior of Great Curassows (Crax rubra), a little‐studied Cracid species currently listed as vulnerable. From 2008 to 2010, we recorded curassows in northwest Costa Rica using both handheld and automated digital recorders. Analysis of recordings revealed that Great Curassows had a vocal repertoire of five call types. Yip and bark calls are sex‐specific alarm calls of short duration (0.12 and 0.08 s, respectively). The descending whistle is a longer duration alarm call (2.18 s) produced primarily by males. The snarl is a short call (0.67 s) associated with a threat display produced by adults with dependent young. The boom call was the most common Great Curassow vocalization, and was given only by males. Boom calls are long (8.86 s), low‐frequency (<150 Hz), multisyllable calls comprised of four stereotyped phrases. Great Curassows often uttered boom calls well before dawn, with a peak in activity at dawn and the hours following. Males produced bouts of repeated boom calls that lasted an average of 35 min, but sometimes continued for more than 5 h. Boom calls were given from February to June, with a peak in late April and early May when breeding begins. Discriminant analysis of boom calls of birds from 10 different locations revealed interindividual variation in call structure that may be useful for bioacoustic monitoring of individuals. Our results suggest that automated recorders might provide a way to monitor the abundance of male curassows because their boom calls are given frequently during the period from February to June and can be detected at distances up to 250 m.     

Contact calls of common marmosets (Callithrix jacchus): influence of age of caller on antiphonal calling and other vocal responses

Marmosets, as do many other primates, live in forest environments, are group living and constantly at risk of predation. Retaining contact with one another is therefore a matter of survival. We ask here whether their contact calls (phee and twitter vocalizations) are in some way ordered acoustically by sex or age and whether the calls of older marmosets elicit different responses than those of younger marmosets. In our study, marmosets (2–14 years) were visually isolated from conspecifics and the vocal responses to each isolated caller by other marmosets in the colony were recorded. Vocal responses to phee calls largely consisted of phee calls and, less commonly, twitter calls. No differences between the responses to calls by males and females were apparent. However, we found a strong positive and significant correlation between the caller's age and the percentage of its phee calls receiving a phee response, and a significant negative correlation between the caller's age and the percentage of its phee calls receiving a twitter response. The older the marmoset, the more antiphonal calling occurred. Two‐syllable phee calls were emitted more often by older marmosets (10–14 years) than by younger ones (2–6 years). Hence, we have found age‐dependent differences in phee‐call production and a consistent change in the response received across the adult life‐span. This age‐dependent effect was independent of kinship relations. This is the first evidence that marmosets distinguish age by vocal parameters alone and make social decisions based on age. Am. J. Primatol. 71:165–170, 2009. © 2008 Wiley‐Liss, Inc.     

The use of Artificial Neural Networks to classify primate vocalizations: a pilot study on black lemurs

The identification of the vocal repertoire of a species represents a crucial prerequisite for a correct interpretation of animal behavior. Artificial Neural Networks (ANNs) have been widely used in behavioral sciences, and today are considered a valuable classification tool for reducing the level of subjectivity and allowing replicable results across different studies. However, to date, no studies have applied this tool to nonhuman primate vocalizations. Here, we apply for the first time ANNs, to discriminate the vocal repertoire in a primate species, Eulemur macaco macaco. We designed an automatic procedure to extract both spectral and temporal features from signals, and performed a comparative analysis between a supervised Multilayer Perceptron and two statistical approaches commonly used in primatology (Discriminant Function Analysis and Cluster Analysis), in order to explore pros and cons of these methods in bioacoustic classification. Our results show that ANNs were able to recognize all seven vocal categories previously described (92.5–95.6%) and perform better than either statistical analysis (76.1–88.4%). The results show that ANNs can provide an effective and robust method for automatic classification also in primates, suggesting that neural models can represent a valuable tool to contribute to a better understanding of primate vocal communication. The use of neural networks to identify primate vocalizations and the further development of this approach in studying primate communication are discussed. Am. J. Primatol. 72:337–348, 2010. © 2009 Wiley‐Liss, Inc.     

Dialects in pygmy marmosets? Population variation in call structure

Population variation in primate vocal structure has been rarely observed. Here, we report significant population differences in the structure of two vocalizations in wild pygmy marmosets (Trills and J calls). We studied 14 groups of pygmy marmosets Callithrix (Cebuella) pygmaea pygmaea from five populations in northeastern Ecuador. We analyzed the acoustic structure of Trills and J calls recorded from two adult animals in each group through focal samples. Although individuals and groups within a population differed in call structure, we found consistent structural differences at a population level for Trills and J calls. Pair‐wise comparisons for the two call types point to San Pablo and Amazoonico as the populations that differed the most, whereas Hormiga and Zancudococha showed the least differences. Discriminant function analysis indicates that calls from each population could be classified accurately at rates significantly above chance. Habitat acoustics, social factors and genetic drift may explain interpopulation vocal differences. This is the first evidence of within‐subspecies vocal differences, or dialects, in wild populations of a neotropical primate species. Am. J. Primatol. 71:333–342, 2009. © 2009 Wiley‐Liss, Inc.     

The use of Vocalizations of the Sambirano Mouse Lemur (<Emphasis Type="Italic">Microcebus sambiranensis</Emphasis>) in an Acoustic Survey of Habitat Preference

Primate vocalizations convey a variety of information to conspecifics. The acoustic traits of these vocalizations are an effective vocal fingerprint to discriminate between sibling species for taxonomic diagnosis. However, the vocal behavior of nocturnal primates has been poorly studied and there are few studies of their vocal repertoires. We compiled a vocal repertoire for the Endangered Sambirano mouse lemur, Microcebus sambiranensis, an unstudied nocturnal primate of northwestern Madagascar, and compared the acoustic properties of one of their call types to those of M. murinus and M. rufus. We recorded vocalizations from radio-collared individuals using handheld recorders over 3 months. We also conducted an acoustic survey to measure the vocal activity of M. sambiranensis in four forest habitat types at the study site. We identified and classified five vocalization types in M. sambiranensis. The vocal repertoires of the three Microcebus species contain very similar call types but have different acoustic properties, with one loud call type, the whistle, having significantly different acoustic properties between species. Our acoustic survey detected more calls of M. sambiranensis in secondary forest, riparian forest, and forest edge habitats, suggesting that individuals may prefer these habitat types over primary forest. Our results suggest interspecific differences in the vocal repertoire of mouse lemurs, and that these differences can be used to investigate habitat preference via acoustic surveys.     

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

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

Individuality in the vocalizations of infant and adult coppery titi monkeys (Plecturocebus cupreus)

As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are short-range and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels: within- and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations.     

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.     

Sex‐biased breeding dispersal is predicted by social environment in birds

Sex‐biased dispersal is common in vertebrates, although the ecological and evolutionary causes of sex differences in dispersal are debated. Here, we investigate sex differences in both natal and breeding dispersal distances using a large dataset on birds including 86 species from 41 families. Using phylogenetic comparative analyses, we investigate whether sex‐biased natal and breeding dispersal are associated with sexual selection, parental sex roles, adult sex ratio (ASR), or adult mortality. We show that neither the intensity of sexual selection, nor the extent of sex bias in parental care was associated with sex‐biased natal or breeding dispersal. However, breeding dispersal was related to the social environment since male‐biased ASRs were associated with female‐biased breeding dispersal. Male‐biased ASRs were associated with female‐biased breeding dispersal. Sex bias in adult mortality was not consistently related to sex‐biased breeding dispersal. These results may indicate that the rare sex has a stronger tendency to disperse in order to find new mating opportunities. Alternatively, higher mortality of the more dispersive sex could account for biased ASRs, although our results do not give a strong support to this explanation. Whichever is the case, our findings improve our understanding of the causes and consequences of sex‐biased dispersal. Since the direction of causality is not yet known, we call for future studies to identify the causal relationships linking mortality, dispersal, and ASR.     

Vocal production in nonhuman primates: Acoustics,physiology, and functional constraints on “honest” advertisement

The physiological mechanisms and acoustic principles underlying sound production in primates are important for analyzing and synthesizing primate vocalizations, for determining the range of calls that are physically producible, and for understanding primate communication in the broader comparative context of what is known about communication in other vertebrates. In this paper we discuss what is known about vocal production in nonhuman primates, relying heavily on models from speech and musical acoustics. We first describe the role of the lungs and larynx in generating the sound source, and then discuss the effects of the supralaryngeal vocal tract in modifying this source. We conclude that more research is needed to resolve several important questions about the acoustics of primate calls, including the nature of the vocal tract's contribution to call production. Nonetheless, enough is known to explore the implications of call acoustics for the evolution of primate communication. In particular, we discuss how anatomy and physiology may provide constraints resulting in “honest” acoustic indicators of body size. © 1995 Wiley-Liss, Inc.     

Does nonnutritive tree gouging in a rainforest‐dwelling lemur convey resource ownership as does loud calling in a dry forest‐dwelling lemur?

Nonhuman primates may defend crucial resources using acoustic or chemical signals. When essential resources are limited, ownership display for a resource may be enhanced. Defending resources may depend on population density and habitat characteristics. Using the Milne Edwards' sportive lemurs (Lepilemur edwardsi) and weasel sportive lemurs (L. mustelinus) as models, we tested whether two cryptic nocturnal lemur species differing in population density and habitat show differences in their vocal and chemical communication for signaling ownership of resources. L. edwardsi inhabits a western dry deciduous forest in a high‐density population, whereas L. mustelinus is found in an eastern rainforest in low density. We followed ten L. edwardsi (six males and four females) and nine L. mustelinus (four males and five females) for 215 hr during the early evening (06:00–10:00 p.m.) and the early morning (02:00–05:00 a.m.) and recorded their behavior using focal animal sampling. We found that both species differed in their vocal and chemical communication. L. edwardsi was highly vocal and displayed loud calling in the mornings and evenings while feeding or in the vicinity of resting places. In contrast, L. mustelinus never vocalized during observations, but displayed tree‐gouging behavior that was never observed in L. edwardsi. Tree gouging occurred more often during early evening sessions than early morning sessions. Subjects gouged trees after leaving their sleeping hole and before moving around. We suggest that, in weasel sportive lemurs, non‐nutritive tree gouging is used as a scent‐marking behavior in order to display ownership of sleeping sites. Altogether, our findings provide first empirical evidence on the evolution of different communication systems in two cryptic nocturnal primate species contrasting in habitat quality and population density. Further investigations are needed to provide more insight into the underlying mechanisms. Am. J. Primatol. 72:1062–1072, 2010. © 2010 Wiley‐Liss, Inc.     

Ontogenetic and Sex Differences Influence Alarm Call Responses in Mammals: a Meta‐Analysis

Animals respond to alarm calls by increasing their antipredator behavior; however, responses may consistently differ by age or sex. Although several adaptive explanations have been proposed to account for age‐dependent antipredator behavior, similar explanations are rarely extended to sex‐specific responses. Furthermore, no attempts have been made to quantitatively estimate the direction or magnitude of these differences across studies. Here, we use meta‐analysis to discover overall trends in the literature, as well as differences owing to experimental or population parameters. Across our sample of available studies (unfortunately biased toward rodents and primates), males respond more than females, and young respond more than adults. Furthermore, young of quickly maturing species display more adult‐like antipredator behavior than young of slowly maturing species, suggesting that young must develop antipredator behavior at a pace consistent with the length of their ontogenetic period (a.k.a. juvenile/sub‐adult period, defined as the time between birth and attainment of sexual maturity). We review previously proposed explanations for such age differences, namely, that longer ontogenetic periods may provide juveniles with time to develop behavior through learning and experience, or, maturation rates may influence age‐specific selection pressures and the consequent evolution of age‐specific behavioral strategies. We evaluate our results in light of these hypotheses, although our conclusions are limited by the number and taxonomic bias of available studies. We therefore suggest ways in which future studies may tease apart the relative importance of learning and experience vs. age‐specific adaptive behavior, and draw attention to opportunities for research on age‐ and sex‐specific alarm call responses.