Revisiting the syntactic abilities of non-human animals: natural vocalizations and artificial grammar learning

The domain of syntax is seen as the core of the language faculty and as the most critical difference between animal vocalizations and language. We review evidence from spontaneously produced vocalizations as well as from perceptual experiments using artificial grammars to analyse animal syntactic abilities, i.e. abilities to produce and perceive patterns following abstract rules. Animal vocalizations consist of vocal units (elements) that are combined in a species-specific way to create higher order strings that in turn can be produced in different patterns. While these patterns differ between species, they have in common that they are no more complex than a probabilistic finite-state grammar. Experiments on the perception of artificial grammars confirm that animals can generalize and categorize vocal strings based on phonetic features. They also demonstrate that animals can learn about the co-occurrence of elements or learn simple 'rules' like attending to reduplications of units. However, these experiments do not provide strong evidence for an ability to detect abstract rules or rules beyond finite-state grammars. Nevertheless, considering the rather limited number of experiments and the difficulty to design experiments that unequivocally demonstrate more complex rule learning, the question of what animals are able to do remains open.     

Call-based species recognition in black-capped chickadees

Species recognition is essential for efficient communication between conspecifics. For this to occur, species information must be unambiguously encoded in the repertoire of each species’ vocalizations. Until now, the study of species recognition in songbirds has been focused mainly on male songs and male territorial behaviour. Species recognition of other learned vocalizations, such as calls, have not been explored, and could prove useful as calls are used in a wider range of contexts. Here, we present an experimental field study investigating the coding of species information in a learned vocalization, the ‘chick-a-dee’ call of the black-capped chickadee (Poecile atricapillus). By modifying natural calls in both temporal and spectral domains and by observing the vocal responses of black-capped chickadees following the playback of these modified calls, we demonstrate that species recognition in chickadees relies on several acoustic features including syntax, frequency modulation, amplitude modulation, and to a lesser extent, call rhythmicity and frequency range.     

Bat echolocation calls facilitate social communication

Bat echolocation is primarily used for orientation and foraging but also holds great potential for social communication. The communicative function of echolocation calls is still largely unstudied, especially in the wild. Eavesdropping on vocal signatures encoding social information in echolocation calls has not, to our knowledge, been studied in free-living bats so far. We analysed echolocation calls of the polygynous bat Saccopteryx bilineata and found pronounced vocal signatures encoding sex and individual identity. We showed experimentally that free-living males discriminate approaching male and female conspecifics solely based on their echolocation calls. Males always produced aggressive vocalizations when hearing male echolocation calls and courtship vocalizations when hearing female echolocation calls; hence, they responded with complex social vocalizations in the appropriate social context. Our study demonstrates that social information encoded in bat echolocation calls plays a crucial and hitherto underestimated role for eavesdropping conspecifics and thus facilitates social communication in a highly mobile nocturnal mammal.     

Temporal rules in vocal exchanges of phees and trills in common marmosets (Callithrix jacchus)

Marmosets exchange two types of calls: phees and trills. We played back phees and trills to investigate the temporal rules of vocal exchanges using ten captive common marmosets (Callithrix jacchus). The marmosets usually emitted the same type of vocalizations just after the stimulus playbacks, and similar regularities were observed in the temporal intervals of phees and in trills. They vocalized with shorter intervals when they responded with trills rather than phees, and, after the first call, they repeatedly vocalized trills with shorter intervals than phees. These results suggest that the temporal rules between phees and trills are qualitatively similar but quantitatively different. These results might be owing to the different distances over which these contact calls are used. Am. J. Primatol. 71:617–622, 2009. © 2009 Wiley‐Liss, Inc.     

Comparison of Neural Responses to Cat Meows and Human Vowels in the Anterior and Posterior Auditory Field of Awake Cats

For humans and animals, the ability to discriminate speech and conspecific vocalizations is an important physiological assignment of the auditory system. To reveal the underlying neural mechanism, many electrophysiological studies have investigated the neural responses of the auditory cortex to conspecific vocalizations in monkeys. The data suggest that vocalizations may be hierarchically processed along an anterior/ventral stream from the primary auditory cortex (A1) to the ventral prefrontal cortex. To date, the organization of vocalization processing has not been well investigated in the auditory cortex of other mammals. In this study, we examined the spike activities of single neurons in two early auditory cortical regions with different anteroposterior locations: anterior auditory field (AAF) and posterior auditory field (PAF) in awake cats, as the animals were passively listening to forward and backward conspecific calls (meows) and human vowels. We found that the neural response patterns in PAF were more complex and had longer latency than those in AAF. The selectivity for different vocalizations based on the mean firing rate was low in both AAF and PAF, and not significantly different between them; however, more vocalization information was transmitted when the temporal response profiles were considered, and the maximum transmitted information by PAF neurons was higher than that by AAF neurons. Discrimination accuracy based on the activities of an ensemble of PAF neurons was also better than that of AAF neurons. Our results suggest that AAF and PAF are similar with regard to which vocalizations they represent but differ in the way they represent these vocalizations, and there may be a complex processing stream between them.     

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.     

Predator‐Associated Vocalizations in North American Red Squirrels (Tamiasciurus hudsonicus): To Whom are Alarm Calls Addressed and How do They Function?

Alarm vocalizations produced by prey species encountering predators can serve a variety of functions. North American red squirrels are a small-bodied mammal popularly known for producing loud, conspicuous alarm calls, but functional accounts of calling in this species are few and contradictory. We conducted research over a 3-yr period on a sample of 47 marked red squirrels in the foothills of the Canadian Rockies. We recorded the production of alarm calls during encounters with natural predators and in a series of simulated predator experiments. We tested for variation in call production patterns consistent with three traditional hypotheses concerning the conspecific warning functions of alarm calling: namely that they serve as warnings to kin, to potential mates, or to territorial neighbors with which callers have an established relationship. Patterns of calling did not provide clear support for any of these hypothesized functions. We consider several possible qualifications to our results. We also consider the possibility that conspicuous calls given by red squirrels during encounters with predators are directed at the predators themselves and function to announce their detection and possibly deter them. This possibility is consistent with additional life-history features of red squirrels including that they are a relatively solitary and territorial, food-hoarding species that produces the same conspicuous vocalizations in response to other squirrels intruding on their territory to steal cones. An important corollary of this account is that red squirrel alarm calls probably do not entail referentially specific messages about different types of predator, as proposed previously.     

Mother-young recognition in an ungulate hider species: a unidirectional process

Parent-offspring recognition is usually crucial for survival of young. In mammals, olfaction often only permits identification at short range, and vocalizations are important at longer distances. Following and hiding antipredator strategies found in newborn mammals may also affect parental recognition mechanisms. We investigated mother-offspring recognition in fallow deer, an ungulate hider species. We analyzed the structure of adult female and fawn contact calls to determine whether they are individually distinctive and tested for mother-offspring recognition. Only females (and not fawns) have individualized vocalizations, with the fundamental frequency as the most distinctive parameter. Playback experiments showed that fawns can distinguish the calls of their mothers from those of other females, but mothers could not discriminate their own and alien fawn calls. Thus, the vocal identification process is unidirectional. In followers, mother-offspring acoustic recognition is mutual, and therefore the different antipredator strategies of newborn mammals may have shaped the modalities of parent-offspring acoustic recognition.     

Acoustic Communication and Sound Degradation: How Do the Individual Signatures of Male and Female Zebra Finch Calls Transmit over Distance?

Background

Assessing the active space of the various types of information encoded by songbirds'' vocalizations is important to address questions related to species ecology (e.g. spacing of individuals), as well as social behavior (e.g. territorial and/or mating strategies). Up to now, most of the previous studies have investigated the degradation of species-specific related information (species identity), and there is a gap of knowledge of how finer-grained information (e.g. individual identity) can transmit through the environment. Here we studied how the individual signature coded in the zebra finch long distance contact call degrades with propagation.

Methodology

We performed sound transmission experiments of zebra finches'' distance calls at various propagation distances. The propagated calls were analyzed using discriminant function analyses on a set of analytical parameters describing separately the spectral and temporal envelopes, as well as on a complete spectrographic representation of the signals.

Results/Conclusion

We found that individual signature is remarkably resistant to propagation as caller identity can be recovered even at distances greater than a hundred meters. Male calls show stronger discriminability at long distances than female calls, and this difference can be explained by the more pronounced frequency modulation found in their calls. In both sexes, individual information is carried redundantly using multiple acoustical features. Interestingly, features providing the highest discrimination at short distances are not the same ones that provide the highest discrimination at long distances.     

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.     

Long-distance communication of acoustic cues to social identity in African elephants

Research on long-distance vocal communication in mammals has tended to focus on the maximum distances over which a vocal signal might be physically detectable. For example, because elephants and some whales communicate using infrasonic calls, and low frequencies are particularly resilient to attenuation, it has often been assumed that these species can communicate over very long distances. However, a wide range of acoustic characteristics typically carry information on individual identity in mammalian calls, and frequency components crucial for social recognition could be distorted or lost as distance from the source increases. We used long-distance playback experiments to show that female African elephants, Loxodonta africana, can recognize a contact call as belonging to a family or bond group member over distances of 2.5 km, but that recognition is more usually achieved over distances of 1-1.5 km. We analysed female contact calls to distinguish source- and filter-related vocal characteristics that have the potential to code individual identity, and rerecorded contact calls 0.5-3.0 km from the loudspeaker to determine how different frequencies persist with distance. Our analyses suggest that the most important frequency components for long-distance communication of social identity may be well above the infrasonic range. When frequency components around 115 Hz become immersed in background noise, once propagation distances exceed 1 km, abilities for long-distance social recognition become limited. Our results indicate that the possession of an unusually long vocal filter, which appears to incorporate the trunk, may be a more important attribute for long-distance signalling in female African elephants than the ability to produce infrasound. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Syntax manipulation changes perception of mobbing call sequences across passerine species

Many species approach predators to harass them and drive them away. Both the intensity of this antipredator strategy and its success are positively related to the size of the group that carries out this mobbing. To recruit individuals to the mob, members of prey species produce mobbing calls. In some songbirds—the Japanese tit, Parus minor, and the southern pied babbler, Turdoides bicolor—mobbing calls are structurally complex and it has been suggested that they convey information by means of compositional syntax, when meaningful items are combined into larger units. These two species combine alert and recruitment calls into an alert and recruitment sequence when attracting conspecifics to cooperate in mobbing a predator. Whether this rudimentary, two‐call, compositional structure is used by other bird species in mobbing calls and how it can alter the ability of heterospecifics to adequately recognize mobbing calls is not well understood. Heterospecifics’ responses to mobs are critical to the success of the mobbing strategy, so it is of great importance to understand whether and how syntax influences these responses. To address these questions, we conducted two playback experiments. Firstly, we investigated whether the great tit, Parus major, extracts different meanings from different individual motifs (i.e., component calls), and from combined motifs in both natural and artificially reversed order. We found that great tits extract different meanings from the two motifs involved in mobbing calls and that they also discriminate for motif order reversal in the mobbing call sequence. Secondly, we investigated whether heterospecifics (the coal tit, Periparus ater, and the common chaffinch, Fringilla coelebs) are sensitive to syntax alteration of great tit mobbing calls. While chaffinches did not respond to great tit mobbing calls, coal tits were sensitive to mobbing call sequence reversal although they did not react in the same way as conspecific subjects. Overall, whereas our results indicate that tits are sensitive to call reversal, this is not to say that tits actually use compositional syntax to increase the information content.     

Ultrasonic courtship vocalizations in wild house mice: spectrographic analyses

House mice emit ultrasonic vocalizations (USVs) during courtship, which are sexually dimorphic and function to attract mates. Spectrographic analyses of laboratory mice show that USVs are surprisingly complex and have features of song. In this study, we conducted the first spectral and temporal analyses of recordings from wild house mice (F1 from wild-caught Mus musculus musculus). Inspection of the spectral shape of syllables shows that the USVs from wild mice can be classified by both frequency and duration, and the most apparent distinction is between low- versus high-frequency calls. High-frequency calls of wild mice seem to be emitted at a much higher frequency range than previously found in some laboratory mice. Interestingly, we found that 20% of males do not vocalize at all, though the reason for their behaviour is unclear. Future studies are needed to determine what kind of information is conveyed in these complex vocalizations, and why some males appear to be non-vocalizers.     

Eavesdropping on the Neighbourhood: Collared Pika (Ochotona collaris) Responses to Playback Calls of Conspecifics and Heterospecifics

The acoustic environment, composed in part by the vocalizations of sympatric animals, is a major source of information and can be used to fine-tune behavioural decisions. Active assessment of alarm calls within and between mammal species is not fully understood. We explored the behavioural responses of collared pikas to con- and heterospecific vocalizations, in order to determine whether they selectively attend to these calls. Pikas increased their vigilance after playback of alarm calls of heterospecific mammals (marmots and ground squirrels), but responded most strongly to conspecific calls. While responses to playback calls of their own, of neighbours and of a stranger did not differ, pikas did discriminate between individual callers in a habituation-discrimination experiment. The ability to make use of information from different sources in their acoustic environment likely facilitates pikas' behavioural decisions that affect foraging, predator avoidance and nepotism.     

The effect of body size and habitat on the evolution of alarm vocalizations in rodents

When confronted with a predator, many mammalian species emit vocalizations known as alarm calls. Vocal structure variation results from the interactive effects of different selective pressures and constraints affecting their production, transmission, and detection. Body size is an important morphological constraint influencing the lowest frequencies that an organism can produce. The acoustic environment influences signal degradation; low frequencies should be favoured in dense forests compared to more open habitats (i.e. the ‘acoustic adaptation hypothesis’). Such hypotheses have been mainly examined in birds, whereas the proximate and ultimate factors affecting vocalizations in nonprimate mammals have received less attention. In the present study, we investigated the relationships between the frequency of alarm calls, body mass, and habitat in 65 species of rodents. Although we found the expected negative relationship between call frequency and body mass, we found no significant differences in acoustic characteristics between closed and open‐habitat species. The results of the present study show that the acoustic frequencies of alarm calls can provide reliable information about the size of a sender in this taxonomic group, although they generally do not support the acoustic adaptation hypothesis.     

Processing of Communication Calls in Guinea Pig Auditory Cortex

Vocal communication is an important aspect of guinea pig behaviour and a large contributor to their acoustic environment. We postulated that some cortical areas have distinctive roles in processing conspecific calls. In order to test this hypothesis we presented exemplars from all ten of their main adult vocalizations to urethane anesthetised animals while recording from each of the eight areas of the auditory cortex. We demonstrate that the primary area (AI) and three adjacent auditory belt areas contain many units that give isomorphic responses to vocalizations. These are the ventrorostral belt (VRB), the transitional belt area (T) that is ventral to AI and the small area (area S) that is rostral to AI. Area VRB has a denser representation of cells that are better at discriminating among calls by using either a rate code or a temporal code than any other area. Furthermore, 10% of VRB cells responded to communication calls but did not respond to stimuli such as clicks, broadband noise or pure tones. Area S has a sparse distribution of call responsive cells that showed excellent temporal locking, 31% of which selectively responded to a single call. AI responded well to all vocalizations and was much more responsive to vocalizations than the adjacent dorsocaudal core area. Areas VRB, AI and S contained units with the highest levels of mutual information about call stimuli. Area T also responded well to some calls but seems to be specialized for low sound levels. The two dorsal belt areas are comparatively unresponsive to vocalizations and contain little information about the calls. AI projects to areas S, VRB and T, so there may be both rostral and ventral pathways for processing vocalizations in the guinea pig.     

Two Novel Vocalizations Are Used by Veeries (Catharus fuscescens) during Agonistic Interactions

Avian vocalizations are common examples of the complex signals used by animals to negotiate during agonistic interactions. In this study, we used two playback experiments to identify agonistic signals in a songbird species with several acoustically complex songs and calls, the veery. In the first experiment, we compared veery singing behavior in response to simulated territorial intrusions including playback of three variations of veery song: 1) song alone as a control, 2) songs with added whisper calls, and 3) songs with introductory notes removed. In the second experiment, we used multimodal stimuli including songs, whisper calls and songs with introductory notes removed, along with a robotic veery mount. Focal males readily responded to all of the playback stimuli, approached the speaker and/or robotic mount, and vocalized. Male veeries gave more whisper calls, and sang more songs without the introductory note in response to all types of playback. However, veeries responded similarly to all types of stimuli presented, and they failed to physically attack the robotic mount. These results indicate that rival veeries use two different types of novel vocalizations: whisper calls and songs lacking the introductory note as agonistic signals, but do not allow us to discern the specific functions of these two vocalizations.     

Mother goats do not forget their kids' calls

Parent-offspring recognition is crucial for offspring survival. At long distances, this recognition is mainly based on vocalizations. Because of maturation-related changes to the structure of vocalizations, parents have to learn successive call versions produced by their offspring throughout ontogeny in order to maintain recognition. However, because of the difficulties involved in following the same individuals over years, it is not clear how long this vocal memory persists. Here, we investigated long-term vocal recognition in goats. We tested responses of mothers to their kids' calls 7-13 months after weaning. We then compared mothers' responses to calls of their previous kids with their responses to the same calls at five weeks postpartum. Subjects tended to respond more to their own kids at five weeks postpartum than 11-17 months later, but displayed stronger responses to their previous kids than to familiar kids from other females. Acoustic analyses showed that it is unlikely that mothers were responding to their previous kids simply because they confounded them with the new kids they were currently nursing. Therefore, our results provide evidence for strong, long-term vocal memory capacity in goats. The persistence of offspring vocal recognition beyond weaning could have important roles in kin social relationships and inbreeding avoidance.     

Primate play vocalizations and their functional significance

It is well known that, among mammals, specific play vocalizations are produced exclusively by certain nonhuman primate species. In order to investigate the functional significance of these calls, we examined their phyletic distribution among New World and Old World monkeys. The results indicate that such calls are produced by species in which allomothering behaviour occurs. We propose a functional explanation of play vocalizations according to which they serve as a possible source of information for maternal retrieval of infants whenever necessary.     

Motivation before meaning: motivational information encoded in meerkat alarm calls develops earlier than referential information

In contrast to historical assumptions about the affective nature of animal vocalizations, it is now clear that many vertebrates are capable of producing specific alarm calls in response to different predators, calls that provide information that goes beyond the motivational state of a caller. However, although these calls function referentially, it does not mean that they are devoid of motivational content. Studies on meerkats (Suricata suricatta) directly support this conclusion. The acoustic structure of their alarm calls simultaneously encodes information that is both motivational (level of urgency) and referential (predator specific). In this study, we investigated whether alarm calls of young meerkats undergo developmental modification and whether the motivational or the referential aspect of calls changes more over time. We found that, based on their acoustic structure, calls of young showed a high correct assignment to low- and high-urgency contexts but, in contrast to adults, low assignment to specific predator types. However, the discrimination among predator types was better in high-urgency than in low-urgency contexts. Our results suggest that acoustic features related to level of urgency are expressed earlier than those related to predator-specific information and may support the idea that referential calls evolve from motivational signals.