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.     

Ethogram and Natural History of Golden-backed Uakaris (<Emphasis Type="Italic">Cacajao melanocephalus</Emphasis>)

We present an ethogram for golden-backed uakaris (Cacajao melanocephalus), based on observations in the field and on a captive individual. We also provide additional observations on the ecology of the wild animals. We studied 3 free-living groups (maximum counts of 5, 15, and 26 individuals) during two wet-seasons (March–July 2007 and January–June 2008) in the flooded igapó forest of Jaú National Park, Amazonas, Brazil. The groups lived in close proximity but never mixed, because river channels separated them. Groups showed fission-fusion behavior, subgroup sizes varied within groups, and we observed 13 different subgroup compositions. The areas used by the groups were ca. 0.82, 2.35, and 2.45 km². We defined a total of 9 behavioral categories. In the wild, the amount of time allocated to the behaviors traveling and foraging/feeding differed between months, but we found no difference in the amount of time devoted to behavioral categories across 3 periods of the day, possibly as a result of the patchy and unpredictable distribution or availability of food patches. Further, the activity patterns varied among groups, perhaps as a reflection of the different group sizes and compositions and different range sizes. We recorded 34 feeding items for wild golden-backed uakaris between January and June 2008, mostly fruits and seeds. No significant variation in the number of different food types occurred across months. We recorded 6 primate species in the study areas. The uakaris neither mobbed nor fled from any other primate species, with the exception of white-fronted capuchin monkeys (Cebus albifrons). In addition, golden-backed uakaris sometimes fled when seeing giant otters (Pteroneura brasiliensis), perhaps indicating that the otters are potential predators of the monkeys. The ethogram and behavioral data provided here increase knowledge of the behavioral ecology of the elusive golden-backed uakari, and will facilitate future comparative studies.     

VOCAL REPERTOIRE OF WILD BREEDING ORANGE-WINGED PARROTS AMAZONA AMAZONICA IN AMAZONIA

ABSTRACT

The vocal repertoire of Amazona amazonica during its breeding season has been recorded from wild individuals in Santa Bárbara do Pará, Pará State, Brazil. At individual nests, we continuously recorded vocalizations and behaviour for four hours in the early morning and three hours in the late afternoon, three times a week throughout the breeding season. We identified nine vocalizations that we classified in three behavioural categories: (1) Flight call—emitted when parrots arrive in the nest area; (2) Perched contact calls—two different vocalizations, one of them related to feeding, were emitted when the pair was perched in the nest area and interacted socially between themselves or with other individuals; (3) Aggressive calls—emitted when birds were in a dangerous situation, i.e. alarm (three types of calls), agonistic contact and distress calls (two types of call). The Orange-winged Parrot is a highly social species and the complexity of its social interactions is reflected in the diversity of its vocal repertoire.     

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 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.     

Vocal Repertoire of Captive Capybara (Hydrochoerus hydrochaeris): Structure,Context and Function

In this work we describe the structure, behavioral context and functionality of the vocal repertoire of capybaras, a social Caviomorph rodent. Additionally, since territoriality is present in this species, we hypothesize the occurrence of vocal differences among social groups. We analyzed a total of 2069 calls emitted by 28 animals from three different social groups. The capybara’s repertoire is comprised by seven call types (whistle, cry, whine, squeal, bark, click and tooth‐chattering). The vocalizations were functionally categorized as contact, alarm, distress and agonistic calls considering their behavioral contexts. The click calls emitted by the adults of the three captive capybara groups were significantly different, confirming our hypothesis of social groups’ vocal differences. The richness of interactions mediated by vocalization in capybaras suggests that the species’ communication is an important mechanism to regulate social encounters and to alert members of the group about environmental cues.     

Ecological and Social Factors Affecting the Vocal Behavior of Adult Female Squirrel Monkeys

Focal recordings of the vocalizations of squirrel monkeys, Saimiri sciureus, occupying an undisturbed Peruvian habitat were collected to evaluate the importance of both the ecological and social functions of female vocal behavior. The rates and sequences of six call types were examined by context: single, double, and multiple chuck, peep, tweet, and tweet-chuck. In contrast to laboratory studies, our findings emphasize the primacy of ecological functions in the wild, where calling permits females to operate as a convoy of spatially separated individuals in an arboreal habitat where visual contact is limited. Chuck calls are probably best interpreted as contact calls. The rate of chucks and tweet-chucks increased when the nearest adult female was > 5 m away. However, call production did not predict a change in the spatial separation between a female and her nearest adult female. During travel, the rate of single and double chucks was greater and the rate of multiple chucks was reduced. No direct relationship was found between foraging activities and vocal behavior. Although secondary, social factors did have a subtle effect on vocal behavior: the larger the social alliance of a female, the lower the rate and repetitiveness of her chuck vocalizations. We also consider the role of variations in vocalization rates among primates and the differing conclusions of field and captive studies of squirrel monkey vocal behavior.     

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.     

Context-related vocalizations in African grey parrots (Psittacus erithacus)

A few animal species are capable of vocal learning. Parrots are well known for their vocal imitation abilities. In this study, we investigated whether African grey parrots (Psittacus erithacus) emit specific vocalizations in specific contexts. We first described the vocal repertoire and its ontogenesis of four captive grey parrots. After a comparison with vocalizations emitted by wild and other captive African grey parrots, we observed that only three call categories were shared by all grey parrots populations, suggesting that isolated populations of parrots develop population-specific calls. Then, we artificially provoked ten different contexts and recorded vocalizations of four captive grey parrots in these situations. Parrots predominantly emitted call categories in some contexts: distress, protestation, alarm, asking (i.e. emitted when a bird wanted something from an experimenter) and contact calls. These results suggest that some calls are learned and can be used in specific contexts.     

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.     

Development of echolocation and communication vocalizations in the big brown bat, <Emphasis Type="Italic">Eptesicus fuscus</Emphasis>

Big brown bats form large maternity colonies of up to 200 mothers and their pups. If pups are separated from their mothers, they can locate each other using vocalizations. The goal of this study was to systematically characterize the development of echolocation and communication calls from birth through adulthood to determine whether they develop from a common precursor at the same or different rates, or whether both types are present initially. Three females and their six pups were isolated from our captive breeding colony. We recorded vocal activity from postnatal day 1 to 35, both when the pups were isolated and when they were reunited with their mothers. At birth, pups exclusively emitted isolation calls, with a fundamental frequency range <20 kHz, and duration >30 ms. By the middle of week 1, different types of vocalizations began to emerge. Starting in week 2, pups in the presence of their mothers emitted sounds that resembled adult communication vocalizations, with a lower frequency range and longer durations than isolation calls or echolocation signals. During weeks 2 and 3, these vocalizations were extremely heterogeneous, suggesting that the pups went through a babbling stage before establishing a repertoire of stereotyped adult vocalizations around week 4. By week 4, vocalizations emitted when pups were alone were identical to adult echolocation signals. Echolocation and communication signals both appear to develop from the isolation call, diverging during week 2 and continuing to develop at different rates for several weeks until the adult vocal repertoire is established.     

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.     

Structural Classification of Wild Boar (Sus scrofa) Vocalizations

Determining whether a species' vocal communication system is graded or discrete requires definition of its vocal repertoire. In this context, research on domestic pig (Sus scrofa domesticus) vocalizations, for example, has led to significant advances in our understanding of communicative functions. Despite their close relation to domestic pigs, little is known about wild boar (Sus scrofa) vocalizations. The few existing studies, conducted in the 1970s, relied on visual inspections of spectrograms to quantify acoustic parameters and lacked statistical analysis. Here, we use objective signal processing techniques and advanced statistical approaches to classify 616 calls recorded from semi‐free ranging animals. Based on four spectral and temporal acoustic parameters—quartile Q25, duration, spectral flux, and spectral flatness—extracted from a multivariate analysis, we refine and extend the conclusions drawn from previous work and present a statistically validated classification of the wild boar vocal repertoire into four call types: grunts, grunt‐squeals, squeals, and trumpets. While the majority of calls could be sorted into these categories using objective criteria, we also found evidence supporting a graded interpretation of some wild boar vocalizations as acoustically continuous, with the extremes representing discrete call types. The use of objective criteria based on modern techniques and statistics in respect to acoustic continuity advances our understanding of vocal variation. Integrating our findings with recent studies on domestic pig vocal behavior and emotions, we emphasize the importance of grunt‐squeals for acoustic approaches to animal welfare and underline the need of further research investigating the role of domestication on animal vocal communication.     

Social vocalizations of big brown bats vary with behavioral context

Bats are among the most gregarious and vocal mammals, with some species demonstrating a diverse repertoire of syllables under a variety of behavioral contexts. Despite extensive characterization of big brown bat (Eptesicus fuscus) biosonar signals, there have been no detailed studies of adult social vocalizations. We recorded and analyzed social vocalizations and associated behaviors of captive big brown bats under four behavioral contexts: low aggression, medium aggression, high aggression, and appeasement. Even limited to these contexts, big brown bats possess a rich repertoire of social vocalizations, with 18 distinct syllable types automatically classified using a spectrogram cross-correlation procedure. For each behavioral context, we describe vocalizations in terms of syllable acoustics, temporal emission patterns, and typical syllable sequences. Emotion-related acoustic cues are evident within the call structure by context-specific syllable types or variations in the temporal emission pattern. We designed a paradigm that could evoke aggressive vocalizations while monitoring heart rate as an objective measure of internal physiological state. Changes in the magnitude and duration of elevated heart rate scaled to the level of evoked aggression, confirming the behavioral state classifications assessed by vocalizations and behavioral displays. These results reveal a complex acoustic communication system among big brown bats in which acoustic cues and call structure signal the emotional state of a caller.     

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.     

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.