Amplitude modulation is a major marker of individual signature in lamb bleats

The source-filter theory of vocal production supports the idea that acoustic signatures are preferentially coded by the fundamental frequency (source-induced variability) and the distribution of energy among the frequency spectrum (filter-induced variability). By investigating the acoustic parameters supporting individuality in lamb bleats, a vocalization which mediates recognition by ewes, here we show that amplitude modulation – an acoustic feature largely independent of the shape of the acoustic tract – can also be an important cue defining an individual vocal signature. Female sheep (Ovis aries) show an acoustic preference for their own lamb. Although playback experiments have shown that this preference is established soon after birth and relies on a unique vocal signature contained in the bleats of the lamb, the physical parameters that encode this individual identity remained poorly identified. We recorded 152 bleats from 13 fifteen-day-old lambs and analyzed their acoustic structure with four complementary statistical methods (ANOVA, potential for individual identity coding PIC, entropy calculation 2^Hs, discriminant function analysis DFA). Although there were slight differences in the acoustic parameters identified by the four methods, it remains that the individual signature relies on both the temporal and frequency domains. The coding of the identity is thus multi-parametric and integrates modulation of amplitude and energy parameters. Specifically, the contribution of the amplitude modulation is important, together with the fundamental frequency F ₀ and the distribution of energy in the frequency spectrum.     

The double vocal signature of crested penguins: is the identity coding system of rockhopper penguins Eudyptes chrysocome due to phylogeny or ecology?

Parent-offspring recognition systems are used in bird colonies to avoid misdirected parental care. In penguins, where the risk of confusion is particularly high, recognition is achieved by acoustic signals that constitute highly efficient vocal signatures. Comparisons between species from the Pygoscelis and Aptenodytes genera have revealed interspecific differences on the encoding of information within the signatures which correlate with the presence/absence of nests in the colonies. However a recent study of individual recognition in macaroni penguins Eudyptes chrysolophus revealed diversity within nest-building species. This paper investigates whether the original and intermediate signature system found in macaroni penguins is shared by another species of Eudyptes , the rockhopper penguin E. chrysocome . Vocal signatures of rockhopper penguins were analysed and compared to macaroni penguins'. We used a methodology derived from the theory of information to determine which parameters of the call were likely to encode individual identity. Playbacks of modified calls in the field complemented the analyses, and parent-chick reunions were compared between the two species. Our results reveal a similar double signature system within the Eudyptes genus, which integrates information simultaneously from the temporal and spectral domains. This double encoding is made through the tempo given by the successive syllables of the call and the harmonic content of the call. While it confirms the hypothesis that signatures are simpler in nest-building species, this result reveals differences in the efficacies of signatures within this category. This suggests that other parameters such as the mean distance recognition should be considered to account for the differences in the encoding of the vocal signatures and in their resulting efficacies.     

Vocal Signature in Wild Infant Chimpanzees

A large array of communication signals supports the fission/fusion social organization in chimpanzees, and among them the acoustic channel plays a large part because of their forest habitat. Adult vocalizations convey social and ecological information to their recipients allowing them to obtain cues about an ongoing event from calls only. In contrast to adult vocalizations, information encoded in infant calls had been hardly investigated. Studies mainly focused on vocal development. The present article aims at assessing the acoustic cues that support individual identity coding in infant chimpanzees. By analyzing recordings performed in the wild from seven 3‐year‐old infant chimpanzees, we showed that their calls support a well‐defined individual vocal signature relying on spectral cues. To assess the reliability of the signature across the calls of an individual, we defined two subsets of recordings on the basis of the characteristics of the frequency modulation (whimpers and screams) and showed that both call types present a reliable vocal signature. Early vocal signature may allow the mother and other individuals in the group to identify the infant caller when visual contact is broken. Chimpanzee mothers may have developed abilities to cope with changing vocal signatures while their infant, still vulnerable, gains in independence in close habitat. Am. J. Primatol. 75:324‐332, 2013. © 2012 Wiley Periodicals, Inc.     

HOW AND WHEN DO LAMBS RECOGNIZE THE BLEATS OF THEIR MOTHERS?

ABSTRACT

In domestic sheep Ovis aries, the mother and the young display a preferential bond for each other that relies on multimodal inter-individual recognition. Lambs show a preference for their own dam shortly after birth, and this is important for their survival. The role of acoustic cues in this early preference for the mother is not clear. The aim of the present work was to analyze the timing of acoustic recognition of the mother and to identify the physical parameters used in the recognition of maternal bleats by the lamb.

In a first study, we investigated the ability of lambs to discriminate between the bleats of their own mother and an alien equivalent mother in a two-choice test. Both ewes were hidden behind a canvas sheet and lambs were not allowed to approach the dams closer than 1 m, thus preventing visual as well as olfactory perception. Tests were conducted 12 hr, 24 hr or 48 hr after birth (n=19 or 20/group). An indication of vocal discrimination was already present at 24 hr and at 48 hr lambs spent significantly more time near their mother than near the alien dam.

In a second step, we investigated which physical parameters of the bleats were important for recognition. For this, we conducted playback experiments with modified bleats at two weeks postpartum. Ours results show that lambs pay attention to a combination of various time, energy and frequency parameters: timbre (distribution of energy within the spectrum), amplitude and frequency modulations appear to be the most important parameters encoding the individual signature.

We conclude that vocal recognition between the ewe and her lamb plays an important role in the display of preferential mother-young bond from very early on. Our studies also demonstrate that the encoding of the individual signature is not limited to the frequency domain but rather involves a multiparametric encoding process.     

Acoustic convergence and divergence in two sympatric burrowing nocturnal seabirds

Shearwaters are nocturnal burrowing seabirds. They return to their colony at dusk and exhibit high vocal activity, underlining the usefulness of acoustic cues to nocturnal communication. The present study aimed to test whether acoustic communication systems of two sympatric shearwater species, the Yelkouan shearwater Puffinus yelkouan and the Mediterranean Cory's shearwater Calonectris diomedea diomedea , converge to similar strategies. Inter-annual mate fidelity and incubation relays led us to focus on sex and individual acoustic signatures. We first characterized those two signatures by analysing the major call emitted by incubating birds. Second, we performed playback experiments to assess ability of birds to vocally discriminate between sexes and mate versus non-mate. The results obtained show that both species use a reliable sex vocal signature supported by frequency and energy features, enabling sex identification of the emitter. By responding only to conspecific same-sex calls, birds may ensure burrow and mate guarding. Conversely, individual vocal signature was mainly supported by temporal parameters, and was more reliable in the Cory's shearwater. Moreover, this species uses vocal exchanges to identify the mate during incubation relays, whereas Yelkouan shearwaters probably need additional cues. In conclusion, we observe an evolutionary convergence in intra-sex communication process but a divergence in mate greeting strategy.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 115–134.     

Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis

As in many anurans, males of the totally aquatic species, Xenopus laevis, advertise their sexual receptivity using vocalizations. Unusually for anurans, X. laevis females also advertise producing a fertility call that results in courtship duets between partners. Although all X. laevis calls consist of repetitive click trains, male and female calls exhibit sex-specific acoustic features that might convey sexual identity. We tested the significance of the carrier frequency and the temporal pattern of calls using underwater playback experiments in which modified calls were used to evoke vocal responses in males. Since males respond differently to male and female calls, the modification of a key component of sexual identity in calls should change the male's response. We found that a female-like slow call rhythm triggers more vocal activity than a male-like fast rhythm. A call containing both a female-like temporal pattern and a female-like carrier frequency elicits higher levels of courtship display than either feature alone. In contrast, a male-like temporal pattern is sufficient to trigger typical male-male encounter vocalizations regardless of spectral cues. Thus, our evidence supports a role for temporal acoustic cues in sexual identity recognition and for spectral acoustic cues in conveying female attractiveness in X. laevis.     

Individually Specific Call Feature Is Not Used to Neighbour-Stranger Discrimination: The Corncrake Case

In various contexts, animals rely on acoustic signals to differentiate between conspecifics. Currently, studies examining vocal signatures use two main approaches. In the first approach, researchers search for acoustic characteristics that have the potential to be individual specific. This approach yields information on variation in signal parameters both within and between individuals and generates practical tools that can be used in population monitoring. In the second approach, playback experiments with natural calls are conducted to discern whether animals are capable of discriminating among the vocal signatures of different individuals. However, both approaches do not reveal the exact signal characteristics that are being used in the discrimination process. In this study, we tested whether an individual-specific call characteristic – namely the length of the intervals between successive maximal amplitude peaks within syllables (PPD) – is crucial in neighbour-stranger discrimination by males of the nocturnal and highly secretive bird species, the corncrake (Crex crex). We conducted paired playback experiments in which corncrakes (n = 47) were exposed to artificial calls with PPD characteristics of neighbour and stranger birds. These artificial calls differed only in PPD structure. The calls were broadcast from a speaker, and we recorded the birds'' behavioural responses. Although corncrakes have previously been experimentally shown to discriminate between neighbours and strangers, we found no difference in the responses to the artificial calls representing neighbours versus strangers. This finding demonstrates that even if vocal signatures are individual specific within a species, it does not automatically mean that said signatures are being crucial in discrimination among individuals. At the same time, the birds'' aggressive responses to the artificial calls indicated that the information transmitted by PPDs is important in species-specific call recognition and may be used by males and/or females to evaluate sender quality, similarly like sound frequency in some insect species.     

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.     

Acoustic recognition in macaroni penguins: an original signature system

Penguins use vocal signatures as cues to identify their kin in dense colonies. Experimental studies of four species in two genera have pointed out that vocal signatures depend on the breeding ecology of the birds. Penguins that have a meeting site for pair members and chicks (genus Pygoscelis), as in many seabirds, have a less complex vocal signature than penguins that have no nests (genus Aptenodytes). To investigate whether this pattern would extend to other nest-building penguins, we studied the vocal signature in a species of the genus Eudyptes, the macaroni penguin, E. chrysolophus. Temporal and spectral features of signatures were analysed to determine which were likely to encode individual identity. Using a methodology derived from the theory of information, we measured and compared the amount of information given by each of these parameters by means of a stereotypy index. We then tested their effective efficiency in playback experiments of modified calls. Like Aptenodytes species, the macaroni penguins used a double coding system that integrated information in both the temporal and spectral domains. The encoding was made through the tempo given by the successive syllables of the call and the harmonic content of the call. However, information was not complementary but was mostly repeated in both domains, and variables were unidimensional as in Pygoscelis signatures. These results point out an original and simple signature system in macaroni penguins. Although they support the hypothesis of simpler systems in nest-building species they also reveal more subtle differences within this category.     

The first call note of the Anhui tree frog (Rhacophorus zhoukaiya) is acoustically suited for enabling individual recognition

The effective production of acoustic signals is critically important for intraspecific communication in vocal animals; however, it is also highly time-consuming, energetically demanding and likely to increase predation risks. Thus, we hypothesized that the biological significance of each component of complex acoustic signals would differ serving specific functions and that the first component of such signals would be most important for social signalling and exhibit unique acoustic characteristics because of the precedence effect. To test this hypothesis, we measured temporal and spectral acoustic parameters for each note in the advertisement calls of the Anhui tree frog (Rhacophorus zhoukaiya), a species in which males build mud burrows and call from within these nests. Multivariate analyses including hierarchical cluster analysis and multidimensional scaling were used, based on temporal and spectral acoustic parameters for each of 10 notes/call. These results show that the first call notes form one cluster while the other notes form a second cluster in multidimensional space when the parameters measured were normalized. Furthermore, the temporal and spectral sound attributes of the first call note provide sufficient information for discrimination between different individuals. Moreover, discriminant analysis showed that the fundamental frequency of the first note is sufficient to identify individuals when the data are not normalized. Taken together, these results indicate that the first call note is poised to play an important role in Anhui tree frog vocal communication insofar as the temporal and spectral features provide sufficient information for individual recognition.     

Flexibility as a Strategy for Avoiding Call Overlap in Male Anhui Treefrogs

Male-male vocal competition is critical for mating success in anuran species; however, it remains unknown that how males regulate their competitive strategies dynamically during competition because calling is highly time-consuming, energetically demanding and likely to increase predation risks. Since different parts of calls will encode different information for vocal communication, we hypothesized that competitive strategies of male frogs may be modulated by the temporal and spectral features of different call notes. To test this hypothesis, the natural advertisement calls(OC), its modified versions with the first call note replaced by white noise(WN) or other notes and with the fifth call note replaced by WN, were played back to the Anhui tree frogs(Rhacophorus zhoukaiyae). Results showed that 1) males produced more competitive calls in response to acoustic stimuli compared to their baseline calling during silence; and 2) males emitted more non-overlapping calls compared to overlapping calls in response to the acoustic stimuli. These results are consistent with the idea that males are flexible to acoustic signals and their competition strategies are modulated dynamically by social contexts.     

Sources of Acoustic Variation in Rhesus Macaque (Macaca mulatta))Vocalizations

All species in the genus Macaca produce a set of harmonically rich vocalizations known as “coos”. Extensive acoustic variation occurs within this call type, a large proportion of which is thought to be associated with different social contexts such as mother-infant separation and the discovery of food. Prior studies of these calls have not taken into account the potential contributions of individual differences and changes in emotional or motivational state. To understand the function of a call and the perceptual salience of different acoustic features, however, it is important to determine the different sources of acoustic variation. I present data on the rhesus macaques' (M. mulatta) coo vocalization and attempt to establish some of the causes of acoustic variation. A large proportion of the variation observed was due to differences between individuals and to putative changes in arousal, not to differences in social context. Specifically, results from a discriminant-function analysis indicated that coo exemplars were accurately assigned to the appropriate individual, but vocal “signatures” were more variable in some contexts than in others. Moreover, vocal signatures may not always be reliable cues to caller identity because closely related individuals sound alike. Rhesus macaque coos evidently provide sufficient acoustic information for individual recognition and possibly kin recognition, but are unlikely to provide sufficient information about an external referent.     

Spectral call features provide information about the aggression level of greater mouse-eared bats (Myotis myotis) during agonistic interactions

Bats rely heavily on acoustic signals in order to communicate with each other in a variety of social contexts. Among those, agonistic interactions and accompanying vocalizations have received comparatively little study. Here, we studied the communicational behaviour between male greater mouse-eared bats (Myotis myotis) during agonistic encounters. Two randomly paired adult males were placed in a box that allowed us to record video and sound synchronously. We describe their vocal repertoire and compare the acoustic structure of vocalizations between two aggression levels, which we quantified via the bats’ behaviour. By inspecting thirty, one-minute long encounters, we identified a rich variety of social calls that can be described as two basic call types: echolocation-like, low-frequency sweeps and long, broadband squawks. Squawks, the most common vocalization, were often noisy, i.e. exhibited a chaotic spectral structure. We further provide evidence for individual signatures and the presence of nonlinear phenomena in this species’ vocal repertoire. As the usage and acoustic structure of vocalizations is known to encode the internal state of the caller, we had predicted that the spectral structure of squawks would be affected by the caller’s aggression level. Confirming our hypothesis, we found that increased aggression positively correlated with an increase in call frequency and tonality. We hypothesize that the extreme spectral variability between and within squawks can be explained by small fluctuations in vocal control parameters (e.g. subglottal pressure) that are caused by the elevated arousal, which is in turn influenced by the aggression level.     

Vocal signature recognition of mothers by fur seal pups

Subantarctic fur seals, Arctocephalus tropicalis, come ashore to breed in dense colonies and lactating females have to alternate foraging trips at sea with periods ashore during which they suckle their pups. The effectiveness of vocal recognition between mothers and pups, has been shown experimentally. To see whether the recognition abilities of females differ from those of their offspring, we investigated how pups recognize their mother's calls. We used artificially modified signals in playback experiments to determine which acoustic parameters support the recognition process. Pups used both the energy spectrum and the ascending frequency modulation occurring at the beginning of each call. However, they seemed to rely mainly on spectral analyses. The vocal identification process at a perceptual level is therefore asymmetrical, as mothers mainly use temporal structures to recognize their pup's calls. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Geographic Variation in the Long Calls of Male Orangutans (Pongo spp.)

Relatively few data exist on population differences in the vocal behavior of mammals. Geographic variation in calls is of special interest because of the implications for resolving evolutionary and behavioral questions. For example, information on geographic variation in vocalizations complements morphological and molecular data used to infer phylogenetic relationships and provides evidence for the mechanisms underlying call development. A quantitative acoustic analysis of orangutan long calls was undertaken, comparing flanged adult males from four geographically distinct sites across Borneo and Sumatra, revealing consistent differences among the calls of individuals. Long calls produced by orangutans from the four sites in Borneo and Sumatra differ in quantitative acoustic measures. Discriminant function analysis reveals that acoustic variables can be used in combination to assign calls to the correct individual, site and island at rates higher than that expected by chance. Specifically, four acoustic parameters proved reliable for distinguishing among the individuals, between sites, and across the two islands that arguably represent populations from separate species or subspecies. Although Bornean and Sumatran long calls share a repetitive structure and show similar call rates (0.100–0.500 LCs/h) and maximum frequency bands (0.400–1.500 kHz), they differ significantly in the number of pulses per call, call speed, call duration, bandwidth, pulse duration, and dominant frequency. Strong consistency in these acoustic parameters is also seen among males within sites and the observed variation may allow for individual recognition. Individual identification by call structure presumably benefits dispersed orangutans, where individuals characteristically forage independently and both encounters and interactions with signaling males are highly variable and largely dependent on context. Acoustic recognition of callers facilitates the choice of which males to join or avoid, thus allowing receivers to manipulate potential costs and benefits of association.     

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.     

At sea vocal repertoire of a foraging seabird

Seabirds spend most of their time at sea, yet our knowledge of their activities and behaviour is limited due to difficulties of in‐situ data collection. In particular, we know virtually nothing about their acoustic communication when at sea. We benefited from the recent development of miniaturised audio‐recording devices to deploy acoustic recorders on breeding Cape gannets Morus capensis to study their vocal activity while foraging. Call sequences were recorded on 1718 occasions, from which acoustic variables were measured on calls with good recording quality. A total of 1348 calls from 18 birds were measured in temporal and frequency domains. Each call was assigned to a behavioural context defined acoustically: sitting on the water, flying, taking off or just before diving. Potential discrimination among calls from different contexts was tested using the random forest algorithm. Within each context, individual stereotypy in the calls was assessed per acoustic variable using a measure of potential of individual coding, and as a combination of variables using a similar multivariate analysis. The acoustic structure differed according to the behavioural context (global accuracy of prediction 75%). Temporal variables (sequence and call duration) were most important to correctly classify the calls among the four contexts. When considering only two contexts, on the water and in the air (merging flying and diving), frequency and spectral variables (percentage of energy below 1200 Hz and fundamental frequency) were of most importance (accuracy 86%). A combination of acoustic variables was necessary to discriminate individuals, but calls from all contexts were not strongly individually distinct (accuracy 41–63%). We provided the first detailed acoustic analysis of a foraging seabird and demonstrated context‐specific acoustic structure in its vocalisations at sea. Our results suggest that seabirds use vocal communication to exchange various types of information that likely improves foraging success.     

Parent-offspring recognition in bank swallows (Riparia riparia): II. Development and acoustic basis

In study 1, bank swallow (Riparia riparia) chicks were exchanged with like-aged chicks from other broods. Parents accepted chicks that were transferred into their nests at age 15 days or younger; rejection began to occur at 16 to 17 days. In study 2, chicks' vocalizations were recorded in the burrow. We found that an immature begging call given by young chicks is replaced by a ‘signature’ call at 15 to 17 days of age. An acoustic analysis suggested that these calls are individually distinctive. Study 3 was a playback experiment designed to test whether the chicks' signature calls are a sufficient cue for parental recognition. We found that parents would approach a speaker broadcasting the calls of their chicks in preference to one simultaneously broadcasting the calls of alien chicks. The pattern of results suggests that parental recognition is based on the chicks' signature calls and that development of recognition is dependent on the development of the call.     

The relationship between perception and production in songbird vocal imitation: what learned calls can teach us

Songbirds produce calls as well as song. This paper summarizes four studies of the zebra finch long call, used by both sexes in similar behavioral contexts. Female long calls are acoustically simpler than male long calls, which include acoustic features learned during development. Production of these male-typical features requires an intact nucleus robustus archistriatalis, the sexually-dimorphic source of the telencephalic projection to brainstem vocal effectors. In experiments that quantified the long calls produced in response to long call playbacks, intact adult zebra finch males, but not females, show a categorical preference for the long calls of females over those of males. Experiments with synthetic stimuli showed that males classify long call stimuli that they hear by gender, using both spectral and temporal information, but that females use only temporal information. Juvenile males (<45 days) did not show the categorical preference, but it emerged during the same period when the robustus archistriatalis matures anatomically and the first male-typical vocalizations are produced. Adult males with robustus archistriatalis lesions lost the categorical preference for female long calls, suggesting that the robustus archistriatalis plays a role in long call discrimination. These results demonstrate that calls complement song as a potent tool for studying the neurobiology of vocal communication.     

Post-natal growth, mother-infant interactions and development of vocalizations in the vespertilionid bat Plecotus auritus

Female brown long-eared bats Plecotus auritus nurse their own young selectively. Choice experiments suggested that females recognized infants by using both olfactory and acoustic cues. Infant isolation calls (i-calls) showed individual variation, and vocal signatures allowed the females to recognize and suckle their own pup. As the pups grew, the i-calls increased in frequency and decreased in duration, and the i-calls appeared to change into orientation cries. Mothers were able to recognize recent calls of their own babies in preference to older calls. Echolocation sounds were distinguishable statistically between lactating females, and the behaviour of the babies during choice experiments suggested that in this species a mutual acoustic recognition occurs. The growth and development of wing shape in P. auritus are described.