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.     

Individual Signature in a Lekking Species: Visual and Acoustic Courtship Parameters May Help Discriminating Conspecifics in the Houbara Bustard

Selection pressures acting on both intrasexual competition and intersexual relationships may lead to the emphasis of individual variation and might thus lead to the expression of individual signature. This is particularly true in lek mating systems, where providing information on identity and/or quality to potential mates or congeners of the same sex can be essential for individuals to optimize their reproductive success. Visual and acoustic signals produced during the courtship of the lekking North African Houbara bustard (Chlamydotis undulata undulata), based on field data from wild birds, are investigated here for the first time. Results show that the vocal signals, called booms, are characterized by a very low frequency, a rare phenomenon in birds which should allow booms to propagate over long distances. Results also show that both visual and acoustic signals are individualized and stereotyped between males. Using three methods of analysis, we highlight the acoustic parameters likely to support vocal individual signature and show that such information mainly relies on frequency parameters.     

Mother-lamb acoustic recognition in sheep: a frequency coding

Ewes of the domestic sheep ( Ovis aries ) display selective maternal investment by restricting care to their own offspring and rejecting alien young. This trait relies on individual recognition processes between ewes and lambs. Whereas identification at the udder is only olfactory, distance recognition is performed through visual and acoustic cues. We studied the effectiveness and modalities of mutual acoustic recognition between ewes and lambs by spectrographic analysis of their vocal signatures and by playbacks of modified calls in the field. Our results show that ewes and their lambs can recognize each other based solely on their calls. The coding of identity within the vocal signatures, previously unknown in sheep, is similar in lamb and ewe: it uses the mean frequency and the spectral energy distribution of the call, namely the timbre of the call. These results point out a simple signature system in sheep that uses only the frequency domain. This engenders a signal with low information content, as opposed to some highly social birds and mammal species that may integrate information both in the temporal and spectral domains. The simplicity of this system is linked to the roles played by vision and olfaction that corroborate the information brought by the vocal signature.     

Individual identity coding depends on call type in the South Polar skua Catharacta maccormicki

In colonial birds, acoustic communication is essential for mate recognition. The South Polar skua (Catharacta maccormicki) lives in loose colonies and is highly territorial for feeding and breeding. We studied the potential of individual identity coding in the three main calls of the South Polar skua repertoire: the courtship, the contact and the alarm calls. We investigated parameters in both temporal and frequencial domains, i.e. amplitude modulation, frequency modulation and power spectrum density. For each parameter, the intra- and inter-individual variabilities were calculated. The ratio between these values represents the potential of individuality coding (PIC) of the considered feature. Low values of PICs for amplitude and frequency modulations show that both parameters may not be used for individual recognition. In contrast, high values of PIC for the power spectrum density indicate that the energy distribution among the frequency spectrum is likely to be an individual marker. PIC also varies according to the call type. Both courtship and contact calls have a higher potentiality of individual identity coding than the alarm call. The two former calls may allow individual recognition whereas the latter may not, and this last result can be extrapolated to many other species.     

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.     

Vocal discrimination of potential mates by female giant pandas (Ailuropoda melanoleuca)

In the current study, we used male giant panda (Ailuropoda melanoleuca) bleats in a habituation–discrimination paradigm to determine whether females discriminate between the vocalizations of different males. We found that females habituated to the bleats of a specific male showed a significant dishabituation when they were presented with bleats from a novel male. Further playbacks, in which we standardized the mean fundamental frequency (pitch) and amplitude modulation of male bleats, indicated that amplitude modulation is the key feature that females attend to when discriminating between male callers. Our results show that female giant pandas can discriminate between the vocalizations of potential mates and provide a platform for further studies investigating the functional role of caller identity in giant panda sexual communication.     

INDIVIDUALITY IN THE VOICE OF FUR SEAL FEMALES: AN ANALYSIS STUDY OF THE PUP ATTRACTION CALL IN ARCTOCEPHALUS TROPICALIS

Like most otariids species, the Subantarctic fur seal breeds on land in large, dense colonies. Pups are confronted by the long and repetitive absences of their mother throughout lactation. At each mother's return, pups have to find her among several hundreds of congeners. This recognition process mainly relies on acoustic signals. We performed an acoustic analysis on 125 calls from 20 females recorded during the 1999–2000 breeding season on Amsterdam Island (Indian Ocean). Ten variables were measured in both temporal and frequency domains. To find the acoustic parameters supporting individual signature, we assessed the differences between individuals using Kruskall-Wallis univariate analysis of variance. For each variable, we also calculated the potential of individuality coding (PIC) as the ratio between the between-individual coefficient of variation and the mean value of the within-individual coefficients of variation. We found that the frequency spectrum, the characteristics of the frequency modulation of the initial and middle part of the call and the call duration exhibit an important individual stereotypy (PIC values ranging between 1.5 and 3), whereas features relative to amplitude and the frequency modulation of the final part of the call are weakly individualized (PIC values between 1 and 1.2).     

Sounds produced by the cichlid fish Metriaclima zebra allow reliable estimation of size and provide information on individual identity

Sounds produced by male cichlids Metriaclima zebra during aggressive interactions were recorded to conduct a detailed analysis and to search for potential individual acoustic signatures. Fish from two different size groups (small and large individuals) were analysed. The two groups were significantly different for all acoustic variables considered; six of seven features demonstrated a significant interindividual variability and most of them were correlated with the size of the emitter. A cross-validated and permuted discriminant function analysis (pDFA) separated the two groups and correctly classified around 50% of the sounds to the correct individuals. Acoustic features that best distinguished among males were the instantaneous frequency of sounds and the modulation of pulse amplitude. These results suggest that acoustic signals could bear information about individual identity. The long-term stability of this signature is likely to be weak since the signature of a growing individual may change over time.     

Vocalisation and its association with androgens and corticosterone in a night frog (Nyctibatrachus humayuni) with unique breeding behaviour

In anurans, vocalisation is used to communicate within and between the sexes during reproduction. Knowledge of vocal repertoire and its diversity is essential in understanding its significance in sexual selection. In this context, we studied the vocal behaviour of Nyctibatrachus humayuni and quantified the urinary metabolites of androgens and corticosterone to understand the associations among hormones, body condition index and vocalisation. Our results show that males of N. humayuni produce an amplitude‐modulated call consisting of a train of pulses. Interestingly, a high degree of inter‐individual variation was observed in the call parameters. The dominant frequency and pulse interval were negatively correlated with male body size, whereas pulse duration and pulse duty cycle were positively correlated with it. Dominant frequency was negatively correlated with androgens and corticosterone, whereas pulse interval was negatively correlated with corticosterone. Further, pulse duty cycle, pulse duration and pulses per call were positively associated with corticosterone. Surprisingly, none of the acoustic parameters was associated with male body temperature and body condition. A significant variation was evident in the vocal effort, dominant frequency and amplitude of advertisement calls produced under different social situations. Calls produced during territory establishment had lower dominant frequency but higher vocal effort, whereas those produced during courtship had higher amplitude and vocal effort than the calls produced in the absence of a competitor/female. Our results suggest that greater inter‐male variability in the advertisement call of N. humayuni could be important in female choice as it may help females to assess the quality of a male. Further, androgens and corticosterone could be important in modulating crucial parameters of the advertisement call.     

Males’ calls carry information about individual identity and morphological characteristics of the caller in burrowing petrels

Acoustic communication in burrowing petrels has been poorly studied. However, as for many other bird species, acoustic communication seems to play an essential role in social interactions during the breeding season of these seabirds. Bachelor males call from their burrow, likely to attract females, but also when vocally challenged by other males. Calling in the breeding colony exposes petrels to high predation risks and thus it should provide an important benefit. The present study focuses on the informative content of males’ calls in the blue petrel Halobaena caerulea and the Antarctic prion Pachyptila desolata, two monogamous petrel species producing a single egg per year. We tested the hypotheses that acoustic parameters of a male's calls 1) reflect phenotypic characteristics, and 2) bear an individual vocal signature. To do so, we first tested on both species the relationships between seven morphometric measurements and 11 acoustic parameters using multivariate analyses. Second, we performed a between‐class analysis and calculated the potential of individuality coding (i.e. the ratio between intra‐ and inter‐individual variabilities) for acoustic parameters in both spectral and temporal domains. Results show acoustic parameters (especially energy quartiles, call duration, and syllable or phrase rate) reflect the caller's body size, bill morphology and wing morphology in both species. Considering the seeming pertinence of wing morphology, we suggest wing area may be a more relevant trait to consider than wing length when studying soaring birds. The results support the idea that energy quartiles, phrase rate and call duration also code for individual identity. Information carried by males’ calls might play a role in social interactions, such as burrow defence (e.g. male‐male competition, neighbour‐stranger discrimination) and/or female mate choice.     

Mother Vocal Recognition in Antarctic Fur Seal Arctocephalus gazella Pups: A Two-Step Process

In otariids, mother’s recognition by pups is essential to their survival since females nurse exclusively their own young and can be very aggressive towards non-kin. Antarctic fur seal, Arctocephalus gazella, come ashore to breed and form dense colonies. During the 4-month lactation period, females alternate foraging trips at sea with suckling period ashore. On each return to the colony, females and pups first use vocalizations to find each other among several hundred conspecifics and olfaction is used as a final check. Such vocal identification has to be highly efficient. In this present study, we investigated the components of the individual vocal signature used by pups to identify their mothers by performing playback experiments on pups with synthetic signals. We thus tested the efficiency of this individual vocal signature by performing propagation tests and by testing pups at different playback distances. Pups use both amplitude and frequency modulations to identify their mother’s voice, as well as the energy spectrum. Propagation tests showed that frequency modulations propagated reliably up to 64m, whereas amplitude modulations and spectral content greatly were highly degraded for distances over 8m. Playback on pups at different distances suggested that the individual identification is a two-step process: at long range, pups identified first the frequency modulation pattern of their mother’s calls, and other components of the vocal signature at closer range. The individual vocal recognition system developed by Antarctic fur seals is well adapted to face the main constraint of finding kin in a crowd.     

Signature whistles in free‐ranging populations of Indo‐Pacific bottlenose dolphins,Tursiops aduncus

Common bottlenose dolphins (Tursiops truncatus) use individually distinctive signature whistles which are highly stereotyped and function as contact calls. Here we investigate whether Indo‐Pacific bottlenose dolphins (T. aduncus) use signature whistles. The frequency trace of whistle contours recorded from three genetically distinct free‐ranging populations was extracted and sorted into whistle types of similar shape using automated categorization. A signature whistle identification method based on the temporal patterns in signature whistle sequences of T. truncatus was used to identify signature whistle types (SWTs). We then compared the degree of variability in SWTs for several whistle parameters to determine which parameters are likely to encode identity information. Additional recordings from two temporarily isolated T. aduncus made during natural entrapment events in 2008 and 2009 were analyzed for the occurrence of SWTs. All populations were found to produce SWTs; 34 SWTs were identified from recordings of free‐ranging T. aduncus and one SWT was prevalent in each recording of the two temporarily isolated individuals. Of the parameters considered, mean frequency and maximum frequency were the least variable and therefore most likely to reflect identity information encoded in frequency modulation patterns. Our results suggest that signature whistles are commonly used by T. aduncus.     

Individual Signature in Canary Songs: Contribution of Multiple Levels of Song Structure

Through variations in features, both within and between individuals, songs of male passerines provide information on the identity of the singer. In domesticated canaries (Serinus canaria), these variations remain, for a large part, to be investigated. This led us to question whether individual identity might be coded at one or more hierarchical levels of song organization, i.e. in acoustic parameters, in the syllable repertoire and in the delivery order of syllables. A song as a whole had numerous individual distinctive acoustic features. However, the structure of its individual signature appeared to be complex. A repertoire combined syllables never sung by other individuals with those shared by other birds. But, most of the individual‐specific syllables that accounted for 16% of a repertoire did not recur frequently. Variation in sequences of multiple syllable types appeared to reflect the individual identity of a male canary. Nearly all sequences larger than three syllable types were specific to the individual that produced them. Some of these occurred recurrently in songs and differed in their acoustic structure between individuals. Focusing upon recurrent sequences might allow vocal recognition of an individual without requiring the knowledge of its full repertoire. However, acoustic parameters and repertoire composition might also serve as additional cues to limit confusion between individuals.     

Calling at the highway: The spatiotemporal constraint of road noise on Pacific chorus frog communication

Loss of acoustic habitat due to anthropogenic noise is a key environmental stressor for vocal amphibian species, a taxonomic group that is experiencing global population declines. The Pacific chorus frog (Pseudacris regilla) is the most common vocal species of the Pacific Northwest and can occupy human‐dominated habitat types, including agricultural and urban wetlands. This species is exposed to anthropogenic noise, which can interfere with vocalizations during the breeding season. We hypothesized that Pacific chorus frogs would alter the spatial and temporal structure of their breeding vocalizations in response to road noise, a widespread anthropogenic stressor. We compared Pacific chorus frog call structure and ambient road noise levels along a gradient of road noise exposures in the Willamette Valley, Oregon, USA. We used both passive acoustic monitoring and directional recordings to determine source level (i.e., amplitude or volume), dominant frequency (i.e., pitch), call duration, and call rate of individual frogs and to quantify ambient road noise levels. Pacific chorus frogs were unable to change their vocalizations to compensate for road noise. A model of the active space and time (“spatiotemporal communication”) over which a Pacific chorus frog vocalization could be heard revealed that in high‐noise habitats, spatiotemporal communication was drastically reduced for an individual. This may have implications for the reproductive success of this species, which relies on specific call repertoires to portray relative fitness and attract mates. Using the acoustic call parameters defined by this study (frequency, source level, call rate, and call duration), we developed a simplified model of acoustic communication space–time for this species. This model can be used in combination with models that determine the insertion loss for various acoustic barriers to define the impact of anthropogenic noise on the radius of communication in threatened species. Additionally, this model can be applied to other vocal taxonomic groups provided the necessary acoustic parameters are determined, including the frequency parameters and perception thresholds. Reduction in acoustic habitat by anthropogenic noise may emerge as a compounding environmental stressor for an already sensitive taxonomic group.     

Individual variation in the booming calls of captive Horned Guans (Oreophasis derbianus): an endangered Neotropical mountain bird

The Horned Guan (Oreophasis derbianus) is a cracid restricted to cloud forests in the Sierra Madre of Chiapas in Mexico and the western-central Mountains in Guatemala. It is an endangered species and urgent conservation measures are required, such as non-invasive monitoring techniques. Here, we study individual features in the boom calls of Horned Guans. Boom calls are acoustic signals used by males during courtship and territorial displays. This call is made of seven notes, divided into two parts: an introductory section characterized by low-amplitude notes and a body section characterized by high-amplitude notes. We recorded 10 males during the breeding seasons of 2010 and 2011 in two captive populations and measured 22 acoustic variables of the calls. We used a combination of statistical analyses to test individuality in Horned Guan vocalizations. Our results showed that time-related variables – but not frequency-related traits – varied between individuals, and that individual calls showed no variation between years. Our results suggest that Horned Guan individuals can be distinguished using fine structural characteristics of their calls and that calls remain stable across years. We argue that such vocal signature could be used to track wild populations as a non-invasive technique in order to improve census data in the short and long term.     

Advertising individual identity by mother and adolescent contact calls in Siberian wapiti Cervus elaphus sibiricus

Individualistic contact calls facilitate mother‐offspring reunion after separation. However, in many mammals, both the acoustic structure and individuality of contact calls differ between mother and young. In contrast, in Siberian wapiti Cervus elaphus sibiricus, contact calls are similar in the acoustics between mother and young, whereas effects of this similarity on vocal individuality were not investigated. In this study, we analyzed acoustic differences between closed‐mouth (nasal) and open‐mouth (oral) contact calls and examined individuality of the most usual oral calls of 19 Siberian wapiti (9 hinds and 10 5–6‐month adolescents) emitted in response to mother‐offspring separation. In the oral calls, the values of frequency and power variables were higher than in the nasal calls. Calls of hinds and adolescents did not differ by the maximum fundamental frequency and duration, whereas the peak frequency was higher in the young. Discriminant function analysis (DFA) based on 11 acoustic variables of oral calls accurately classified to individual 92.5% of hind calls and 96.9% of adolescent calls (chi‐square test for differences between hinds and adolescents, p = 0.19). Variables mainly contributing to vocal identity (duration, start, and maximum fundamental frequency) were the same in calls of mothers and adolescents. We conclude that similarities in the acoustics calls of mothers and adolescents mean that they do not differ in their potential for encoding individual identity, suggesting a mutual process of mother‐offspring vocal recognition in Siberian wapiti.     

Processing of behaviorally relevant temporal parameters of acoustic stimuli by single neurons in the superior olivary nucleus of the leopard frog

Summary Response characteristics of 130 single neurons in the superior olivary nucleus of the northern leopard frog (Rana pipiens pipiens) were examined to determine their selectivity to various behaviorally relevant temporal parameters [rise-fall time, duration, and amplitude modulation (AM) rate of acoustic signals. Response functions were constructed with respect to each of these variables. Neurons with different temporal firing patterns such as tonic, phasic or phasic-burst firing patterns, participated in time domain analysis in specific manners. Phasic neurons manifested preferences for signals with short rise-fall times, thus possessing low-pass response functions with respect to this stimulus parameter; conversely, tonic and phasic-burst units were non-selective and possessed all-pass response functions. A distinction between temporal firing patterns was also observed for duration coding. Whereas phasic units showed no change in the mean spike count with a change in stimulus duration (i.e., all-pass duration response functions), tonic and phasic-burst units gave higher mean spike counts with an increase in stimulus duration (i.e., primary-like high-pass response functions). Phasic units manifested greater response selectivity for AM rate than did tonic or phasic-burst units, and many phasic units were tuned to a narrow range of modulation rates (i.e., band-pass). The results suggest that SON neurons play an important role in the processing of complex acoustic patterns; they perform extensive computations on AM rate as well as other temporal parameters of complex sounds. Moreover, the response selectivities for rise-fall time, duration, and AM rate could often be shown to contribute to the differential responses to complex synthetic and natural sounds.Abbreviations SON superior olivary nucleus - DMN dorsal medullary nucleus - TS torus semicircularis - FTC frequency threshold curve - BF best excitatory frequency - PAM pulsatile amplitude modulation - SAM sinusoidal amplitude modulation - SQAM square-wave amplitude modulation - MTF modulation transfer function - PSTH peri-stimulus time histogram     

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.     

SIGNAL™/RTSD™ SOUND ANALYSIS SYSTEM

ABSTRACT

The prevalence of complex acoustic structures in mammalian vocalisations can make it difficult to quantify frequency characteristics. We describe two methods developed for the frequency analysis of a complex swift fox Vulpes velox vocalisation, the barking sequence: (1) autocorrelation function analysis and (2) instantaneous frequency analysis. The autocorrelation function analysis results in an energy density spectrum of the signal's averaged amplitude and frequency information. This analysis was used for locating possible formant structures and quantifying the energy distribution of single barks in the barking sequence. The instantaneous frequency analysis is applied to individual continuous frequency bands and generates frequency contours with a resolution of a couple of Hertz. It was used to quantify frequency modulation and calculate average frequencies of harmonic bands in individual barks and to estimate fundamental frequencies. This second method of analysis had to be evaluated with spectrographic analysis to gauge its reliability for each band analysed. The algorithms used should make both of these methods applicable to other complex vocalisations.     

Discrimination of sinusoidally frequency-modulated sound signals mimicking species-specific communication calls in the FM-bat Phyllostomus discolor

In the lesser spear-nosed bat, Phyllostomus discolor, maternal directive calls are characterized by an individual type of sinusoidal frequency modulation (= SFM) pattern. Beside modulation frequency, modulation depth, carrier frequency, and number of modulation cycles per call contribute to the mother's vocal signature. Since juvenile P. discolor learn to adapt their isolation calls to the corresponding call characteristics of the own mother or even to playback of a computer-stored directive call, if hand-reared in the absence of conspecifics, the bats' auditory system ought to be able to resolve interindividual differences in communication call structure. However, quantitative psychoacoustic data on the discrimination of SFM signals in this species are not available. Thus, in the present study, lesser spear-nosed bats were trained in a two-alternative forced-choice procedure to discriminate between two alternatingly presented SFM sound signals differing in modulation frequency. Other characteristics of acoustic stimuli were identical and designed to mimick the fundamental of species-specific calls. By gradually reducing the difference in modulation frequency between both stimuli within the behavioural relevant range until the animals' performance dropped below the 75%-correct level, a considerable auditory spectro-temporal resolution has been revealed. Particularly in comparison to the overall interindividual variation of this call parameter (minimal modulation frequency = 49 Hz, maximum = 100 Hz), the determined average difference limen for modulation frequency of 2.42 ± 0.29 Hz seems substantial and sufficient for labelling individuals. Accepted: 30 November 1996