Investigating the potential for call combinations in a lifelong vocal learner

The ability for humans to create seemingly infinite meaning from a finite set of sounds has likely been a critical component in our success as a species, allowing the unbounded communication of information. Syntax, the combining of meaningful sounds into phrases, is one of the primary features of language that enables this extensive expressivity. The evolutionary history of syntax, however, remains largely debated, and it is only very recently that comparative data for syntax in animals have been revealed. Here, we provide further evidence for a structural basis of potential syntactic‐like call combinations in the vocal communication system of a group‐living songbird. Acoustic analyses indicate that Western Australian magpies (Gymnorhina tibicen dorsalis) structurally combine generic alarm calls with acoustically distinct alert calls to produce an alarm alert sequence. These results are distinct from previous examples of call combinations as, to our knowledge, evidence for this capacity is yet to be demonstrated in the natural communication of a non‐human species that is capable of vocal learning throughout life. These findings offer prospects for experimental investigation into the presence and function of magpie call combinations, extending our understanding of animal vocal complexity.     

The significant features of Japanese macaque coo sounds: a psychophysical study

Japanese macaques, Macaca fuscata, were trained with a positive reinforcement operant procedure to discriminate smooth early high and smooth late high coo sounds recorded during Green's (1975) field study of the speices' vocal repertoire. Subjects labelled the various tokens by maintaining contact with a response device for calls from one category and by breaking contact for those of the second call type. After the completion of discrimination training, the generalization of the operant behaviour to novel natural and synthetic vocalizations was measured. Initial generalization tests established that macaques would respond appropriately both to natural vocalizations and to computer-synthesized prototypes representing the smooth early high-smooth late high contrast. In subsequent tests, individual acoustic features were removed from the synthetic prototypes to determine the minimal elements of functional coo sounds. These tests suggested that those sounds are distinguished by the predominant direction of their frequency change which, in turn, is determined by the temporal position of their highest frequency.     

Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls

Biological invasions are a major threat to biodiversity. Invasive species that use acoustic communication can affect native species through interference in the acoustic niche. The American Bullfrog Lithobates catesbeianus is a highly invasive anuran that is widely distributed in the Brazilian Atlantic Rainforest. Adult male bullfrogs emit loud advertisement calls at frequencies that overlap with the calls of several native species of frogs. Given that spectral overlap is a major factor in acoustic masking, the purpose of this study was to test the effects of the acoustic invasion of L. catesbeianus on native frogs that have calls with and without spectral overlap with the invader. In field experiments, we exposed calling males of two overlapping species and two non-overlapping species to recorded bullfrog vocalizations, white noise, and the vocalization of another native frog species. To identify effects, we compared calls recorded before, during, and after exposure. Our results showed that native species altered their calls in response to the bullfrog calls. However, we also observed similar responses to white noise and heterospecific native calls. Both the invasive and heterospecific calls were emitted at low frequencies, which suggests that the observed responses might be specific to low-frequency calls. Our results provide evidence that the introduction of new sounds can cause native species to modify their calls, and that responses to exogenous sounds are species- and stimulus-specific.     

ACOUSTIC COMMUNICATION SIGNALS OF MYSTICETE WHALES

ABSTRACT

Mysticete (baleen) whales produce a variety of vocalizations and sounds, but relatively few of these have been well described with accompanying behavior. This review concentrates on the vocalizations consistently associated with behavioral interactions or acoustic exchanges between or among conspecifics. These communication “signals” have been categorized for this review as contact calls of single animals outside of the breeding season (including cow-calf pairs), vocalizations reported during the breeding season (often designated as “songs”), and calls produced by active groups of whales that may or may not have a reproductive function. While much remains unknown, the data obtained thus far indicate that the social vocalizations of baleen whales have structural/functional similarities with those of other mammals and birds.     

Acoustic signals of a solitary subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae): physical characteristics and behavioural correlates

The purpose of this study was to analyse and describe vocalizations of a solitary subterranean rodent, Ctenomys talarum. In adult C. talarum five different sounds (four true vocalizations and one mechanical sound) were recorded during different behavioural contexts. Using data from the laboratory and literature, we classified these vocalizations as territorial, distress, and mating calls. We found that the vocalization range in C. talarum is shifted towards low frequencies, which transmit better in underground burrows and match well the hearing range described for other species of subterranean rodents. These low-frequency vocalizations, also found in other non-related subterranean rodents, may reflect an adaptation to the acoustic conditions of the habitat. Electronic Publication     

Campbell's Monkeys Use Affixation to Alter Call Meaning

Human language has evolved on a biological substrate with phylogenetic roots deep in the primate lineage. Here, we describe a functional analogy to a common morphological process in human speech, affixation, in the alarm calls of free-ranging adult Campbell''s monkeys (Cercopithecus campbelli campbelli). We found that male alarm calls are composed of an acoustically variable stem, which can be followed by an acoustically invariable suffix. Using long-term observations and predator simulation experiments, we show that suffixation in this species functions to broaden the calls'' meaning by transforming a highly specific eagle alarm to a general arboreal disturbance call or by transforming a highly specific leopard alarm call to a general alert call. We concluded that, when referring to specific external events, non-human primates can generate meaningful acoustic variation during call production that is functionally equivalent to suffixation in human language.     

Representation of complex vocalizations in the Lusitanian toadfish auditory system: evidence of fine temporal,frequency and amplitude discrimination

Many fishes rely on their auditory skills to interpret crucial information about predators and prey, and to communicate intraspecifically. Few studies, however, have examined how complex natural sounds are perceived in fishes. We investigated the representation of conspecific mating and agonistic calls in the auditory system of the Lusitanian toadfish Halobatrachus didactylus, and analysed auditory responses to heterospecific signals from ecologically relevant species: a sympatric vocal fish (meagre Argyrosomus regius) and a potential predator (dolphin Tursiops truncatus). Using auditory evoked potential (AEP) recordings, we showed that both sexes can resolve fine features of conspecific calls. The toadfish auditory system was most sensitive to frequencies well represented in the conspecific vocalizations (namely the mating boatwhistle), and revealed a fine representation of duration and pulsed structure of agonistic and mating calls. Stimuli and corresponding AEP amplitudes were highly correlated, indicating an accurate encoding of amplitude modulation. Moreover, Lusitanian toadfish were able to detect T. truncatus foraging sounds and A. regius calls, although at higher amplitudes. We provide strong evidence that the auditory system of a vocal fish, lacking accessory hearing structures, is capable of resolving fine features of complex vocalizations that are probably important for intraspecific communication and other relevant stimuli from the auditory scene.     

Vocal Ontogeny in Neotropical Singing Mice (Scotinomys)

Isolation calls produced by dependent young are a fundamental form of communication. For species in which vocal signals remain important to adult communication, the function and social context of vocal behavior changes dramatically with the onset of sexual maturity. The ontogenetic relationship between these distinct forms of acoustic communication is surprisingly under-studied. We conducted a detailed analysis of vocal development in sister species of Neotropical singing mice, Scotinomys teguina and S. xerampelinus. Adult singing mice are remarkable for their advertisement songs, rapidly articulated trills used in long-distance communication; the vocal behavior of pups was previously undescribed. We recorded 30 S. teguina and 15 S. xerampelinus pups daily, from birth to weaning; 23 S. teguina and 11 S. xerampelinus were recorded until sexual maturity. Like other rodent species with poikilothermic young, singing mice were highly vocal during the first weeks of life and stopped vocalizing before weaning. Production of first advertisement songs coincided with the onset of sexual maturity after a silent period of ≧2 weeks. Species differences in vocal behavior emerged early in ontogeny and notes that comprise adult song were produced from birth. However, the organization and relative abundance of distinct note types was very different between pups and adults. Notably, the structure, note repetition rate, and intra-individual repeatability of pup vocalizations did not become more adult-like with age; the highly stereotyped structure of adult song appeared de novo in the first songs of young adults. We conclude that, while the basic elements of adult song are available from birth, distinct selection pressures during maternal dependency, dispersal, and territorial establishment favor major shifts in the structure and prevalence of acoustic signals. This study provides insight into how an evolutionarily conserved form of acoustic signaling provides the raw material for adult vocalizations that are highly species specific.     

Food-Associated Calling in Gorillas (Gorilla g. gorilla) in the Wild

Many nonhuman primates produce food-associated vocalizations upon encountering or ingesting particular food. Concerning the great apes, only food-associated vocalizations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have been studied in detail, providing evidence that these vocalizations can be produced flexibly in relation to a variety of factors, such as the quantity and quality of food and/or the type of audience. Only anecdotal evidence exists of eastern (Gorilla beringei) and western gorillas (Gorilla gorilla) producing food-associated vocalizations, termed singing or humming. To enable a better understanding of the context in which these calls are produced, we investigated and compared the vocal behavior of two free-ranging groups of western lowland gorillas (Gorilla g. gorilla) at Mondika, Republic of Congo. Our results show that (a) food-associated call production occurs only during feeding and not in other contexts; (b) calling is not uniformly distributed across age and sex classes; (c) calls are only produced during feeding on specific foods; and (d) normally just one individual gives calls during group feeding sessions, however, certain food types elicit simultaneous calling of two or more individuals. Our findings provide new insight into the vocal abilities of gorillas but also carry larger implications for questions concerning vocal variability among the great apes. Food-associated calls of nonhuman primates have been shown to be flexible in terms of when they are used and who they are directed at, making them interesting vocalizations from the viewpoint of language evolution. Food-associated vocalizations in great apes can offer new opportunities to investigate the phylogenetic development of vocal communication within the primate lineage and can possibly contribute novel insights into the origins of human language.     

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.     

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.     

Individual Distinctiveness in Call Types of Wild Western Female Gorillas

Individually distinct vocalizations play an important role in animal communication, allowing call recipients to respond differentially based on caller identity. However, which of the many calls in a species'' repertoire should have more acoustic variability and be more recognizable is less apparent. One proposed hypothesis is that calls used over long distances should be more distinct because visual cues are not available to identify the caller. An alternative hypothesis proposes that close calls should be more recognizable because of their importance in social interactions. To examine which hypothesis garners more support, the acoustic variation and individual distinctiveness of eight call types of six wild western gorilla (Gorilla gorilla) females were investigated. Acoustic recordings of gorilla calls were collected at the Mondika Research Center (Republic of Congo). Acoustic variability was high in all gorilla calls. Similar high inter-individual variation and potential for identity coding (PIC) was found for all call types. Discriminant function analyses confirmed that all call types were individually distinct (although for call types with lowest sample size - hum, grumble and scream - this result cannot be generalized), suggesting that neither the distance at which communication occurs nor the call social function alone can explain the evolution of identity signaling in western gorilla communication.     

Development of Early Vocalizations and the Chick-a-dee Call in the Black-capped Chickadee,Parus atricapillus

The chick-a-dee call of the black-capped chickadee (Parus atricapillus) is composed of discrete elements, or notes, that are combined to form hundreds of different calls. To investigate the development of this complex call, 12 families of color-marked chickadees were observed and recorded in the wild. Vocalizations were monitored for 18 d in the nest and 14–18 d postfledging. Most vocalizations of nestlings and fledglings were associated with feeding. At hatching, vocalizations consisted of a structurally simple note type that became more complex and variable with age. Around 9–12 d, the development of the call occurred, when single notes became organized into a multiple-note unit. Notes within the call differentiated into higher frequency, rapidly modulated initial note types and a lower frequency, moderately modulated terminal note type, features also present in adult chick-a-dee calls. Several adult-like calls including chick-a-dee calls, fee-bee songs, and a subsong-like vocalization developed prior to fledgling dispersal. Based on resemblances of note structure and general call structure, the chick-a-dee call appeared to develop from calls of nestlings and fledglings, although not necessarily in a chronologically linear progression. Some features of the chick-a-dee call closely resembled features of older nestling and fledgling calls, while other features more closely resembled the sounds of very young nestlings. Vocal development in the chickadee is compared with song and call development in other species, and the possible significance of acoustic resemblances between chick-a-dee calls and the food-associated calls of nestlings and fledglings is discussed.     

Calls during agonistic interactions vary with arousal and raise audience attention in ravens

Background

Acoustic properties of vocalizations can vary with the internal state of the caller, and may serve as reliable indicators for a caller’s emotional state, for example to prevent conflicts. Thus, individuals may associate distinct characteristics in acoustic signals of conspecifics with specific social contexts, and adjust their behaviour accordingly to prevent escalation of conflicts. Common ravens (Corvus corax) crowd-forage with individuals of different age classes, sex, and rank, assemble at feeding sites, and engage in agonistic interactions of varying intensity. Attacked individuals frequently utter defensive calls in order to appease the aggressor. Here, we investigated if acoustic properties of defensive calls change with varying levels of aggression, and if bystanders respond to these changes.

Results

Individuals were more likely to utter defensive calls when the attack involved contact aggression, and when the attacker was higher in rank than the victim. Defensive calls produced during intense conflicts were longer and uttered at higher rates, and showed higher fundamental frequency- and amplitude-related measures than calls uttered during low-intensity aggression, indicating arousal-based changes in defensive calls. Playback experiments showed that ravens were more likely to react in response to defensive calls with higher fundamental frequency by orientating towards the speakers as compared to original calls and calls manipulated in duration.

Conclusions

Arousal-based changes are encoded in acoustic parameters of defensive calls in attacked ravens, and bystanders in the audience pay attention to the degree of arousal in attacked conspecifics. Our findings imply that common ravens can regulate conflicts with conspecifics by means of vocalizations, and are able to gather social knowledge from conspecific calls.

     

Dialects in southern Rocky Mountain pikas, Ochotona princeps (Lagomorpha)

This work quantifies the geographic variation (dialects) in the vocalizations of southern Rocky Mountain pikas and presents data on the vocal responses of pikas to playback of recorded vocalizations of two dialects. Pika vocalizations were tape-recorded in twenty-six locations in Wyoming, Colorado, Utah and New Mexico. Two dialects (based on duration of note and frequency of fundamental) were found in short calls. One dialect was north of the Colorado River (dialect A), and the other was south of the Colorado River (dialect B). There was seasonal variation in the incidence of vocalizations with a peak of songs in late spring and a peak of short calls in late summer. Results of this study indicate that acoustic characteristics of vocalizations could be a useful taxonomic tool in the genus Ochotona.     

Grouping in auditory temporal perception and vocal production is mutually adapted: the case of wriggling calls of mice

Auditory Gestalt perception by grouping of species-specific vocalizations to a perceptual stream with a defined meaning is typical for human speech perception but has not been studied in non-human mammals so far. Here we use synthesized models of vocalizations (series of wriggling calls) of mouse pups (Mus domesticus) and show that their mothers perceive the call series as a meaningful Gestalt for the release of instinctive maternal behavior, if the inter-call intervals have durations of 100–400 ms. Shorter or longer inter-call intervals significantly reduce the maternal responsiveness. We also show that series of natural wriggling calls have inter-call intervals mainly in the range of 100–400 ms. Thus, series of natural wriggling calls of pups match the time-domain auditory filters of their mothers in order to be optimally perceived and recognized. A similar time window exists for the production of human speech and the perception of series of sounds by humans. Neural mechanisms for setting the boundaries of the time window are discussed.     

The structure of innate vocalizations in Foxp2‐deficient mouse pups

Heterozygous mutations of the human FOXP2 gene are implicated in a severe speech and language disorder. Aetiological mutations of murine Foxp2 yield abnormal synaptic plasticity and impaired motor‐skill learning in mutant mice, while knockdown of the avian orthologue in songbirds interferes with auditory‐guided vocal learning. Here, we investigate influences of two distinct Foxp2 point mutations on vocalizations of 4‐day‐old mouse pups (Mus musculus). The R552H missense mutation is identical to that causing speech and language deficits in a large well‐studied human family, while the S321X nonsense mutation represents a null allele that does not produce Foxp2 protein. We ask whether vocalizations, based solely on innate mechanisms of production, are affected by these alternative Foxp2 mutations. Sound recordings were taken in two different situations: isolation and distress, eliciting a range of call types, including broadband vocalizations of varying noise content, ultrasonic whistles and clicks. Sound production rates and several acoustic parameters showed that, despite absence of functional Foxp2, homozygous mutants could vocalize all types of sounds in a normal temporal pattern, but only at comparably low intensities. We suggest that altered vocal output of these homozygotes may be secondary to developmental delays and somatic weakness. Heterozygous mutants did not differ from wild‐types in any of the measures that we studied (R552H ) or in only a few (S321X ), which were in the range of differences routinely observed for different mouse strains. Thus, Foxp2 is not essential for the innate production of emotional vocalizations with largely normal acoustic properties by mouse pups.     

The Acoustic Properties of Low Intensity Vocalizations Match Hearing Sensitivity in the Webbed-Toed Gecko,Gekko subpalmatus

The design of acoustic signals and hearing sensitivity in socially communicating species would normally be expected to closely match in order to minimize signal degradation and attenuation during signal propagation. Nevertheless, other factors such as sensory biases as well as morphological and physiological constraints may affect strict correspondence between signal features and hearing sensitivity. Thus study of the relationships between sender and receiver characteristics in species utilizing acoustic communication can provide information about how acoustic communication systems evolve. The genus Gekko includes species emitting high-amplitude vocalizations for long-range communication (loud callers) as well as species producing only low-amplitude vocalizations when in close contact with conspecifics (quiet callers) which have rarely been investigated. In order to investigate relationships between auditory physiology and the frequency characteristics of acoustic signals in a quiet caller, Gekko subpalmatus we measured the subjects’ vocal signal characteristics as well as auditory brainstem responses (ABRs) to assess auditory sensitivity. The results show that G. subpalmatus males emit low amplitude calls when encountering females, ranging in dominant frequency from 2.47 to 4.17 kHz with an average at 3.35 kHz. The auditory range with highest sensitivity closely matches the dominant frequency of the vocalizations. This correspondence is consistent with the notion that quiet and loud calling species are under similar selection pressures for matching auditory sensitivity with spectral characteristics of vocalizations.