Vocal tract anatomy of king penguins: morphological traits of two-voiced sound production.

BACKGROUND: The astonishing variety of sounds that birds can produce has been the subject of many studies aiming to identify the underlying anatomical and physical mechanisms of sound production. An interesting feature of some bird vocalisations is the simultaneous production of two different frequencies. While most work has been focusing on songbirds, much less is known about dual-sound production in non-passerines, although their sound production organ, the syrinx, would technically allow many of them to produce "two voices". Here, we focus on the king penguin, a colonial seabird whose calls consist of two fundamental frequency bands and their respective harmonics. The calls are produced during courtship and for partner and offspring reunions and encode the birds' identity. We dissected, µCT-scanned and analysed the vocal tracts of six adult king penguins from Possession Island, Crozet Archipelago. RESULTS: King penguins possess a bronchial type syrinx that, similarly to the songbird's tracheobronchial syrinx, has two sets of vibratory tissues, and thus two separate sound sources. Left and right medial labium differ consistently in diameter between 0.5 and 3.2%, with no laterality between left and right side. The trachea has a conical shape, increasing in diameter from caudal to cranial by 16%. About 80% of the king penguins' trachea is medially divided by a septum consisting of soft elastic tissue (septum trachealis medialis). CONCLUSIONS: The king penguins' vocal tract appears to be mainly adapted to the life in a noisy colony of a species that relies on individual vocal recognition. The extent between the two voices encoding for individuality seems morphologically dictated by the length difference between left and right medial labium. The septum trachealis medialis might support this extent and could therefore be an important anatomical feature that aids in the individual recognition process.

Explosive breeding in tropical anurans: environmental triggers, community composition and acoustic structure.

BACKGROUND: Anurans largely rely on acoustic communication for sexual selection and reproduction. While multiple studies have focused on the calling activity patterns of prolonged breeding assemblages, species that concentrate their reproduction in short-time windows, explosive breeders, are still largely unknown, probably because of their ephemeral nature. In tropical regions, multiple species of explosive breeders may simultaneously aggregate leading to massive, mixed and dynamic choruses. To understand the environmental triggers, the phenology and composition of these choruses, we collected acoustic and environmental data at five ponds in French Guiana during a rainy season, assessing acoustic communities before and during explosive breeding events. RESULTS: We detected in each pond two explosive breeding events, lasting between 24 and 70 h. The rainfall during the previous 48 h was the most important factor predicting the emergence of these events. During explosive breeding events, we identified a temporal factor that clearly distinguished pre- and mid-explosive communities. A common pool of explosive breeders co-occurred in most of the events, namely Chiasmocleis shudikarensis, Trachycephalus coriaceus and Ceratophrys cornuta. Nevertheless, the species composition was remarkably variable between ponds and for each pond between the first and the second events. The acoustic structure of explosive breeding communities had outlying levels of amplitude and unexpected low acoustic diversity, significantly lower than the communities preceding explosive breeding events. CONCLUSIONS: Explosive breeding communities were tightly linked with specific rainfall patterns. With climate change increasing rainfall variability in tropical regions, such communities may experience significant shifts in their timing, distribution and composition. In structurally similar habitats, located in the same region without obvious barriers, our results highlight the variation in composition across explosive breeding events. The characteristic acoustic structure of explosive breeding events stands out from the circadian acoustic environment being easily detected at long distance, probably reflecting behavioural singularities and conveying heterospecific information announcing the availability of short-lived breeding sites. Our data provides a baseline against which future changes, possibly linked to climate change, can be measured, contributing to a better understanding on the causes, patterns and consequences of these unique assemblages.

How minute sooglossid frogs hear without a middle ear.

Acoustic communication is widespread in animals. According to the sensory drive hypothesis [Endler JA (1993) Philos Trans R Soc Lond B Biol Sci 340(1292):215-225], communication signals and perceptual systems have coevolved. A clear illustration of this is the evolution of the tetrapod middle ear, adapted to life on land. Here we report the discovery of a bone conduction-mediated stimulation of the ear by wave propagation in Sechellophryne gardineri, one of the world's smallest terrestrial tetrapods, which lacks a middle ear yet produces acoustic signals. Based on X-ray synchrotron holotomography, we measured the biomechanical properties of the otic tissues and modeled the acoustic propagation. Our models show how bone conduction enhanced by the resonating role of the mouth allows these seemingly deaf frogs to communicate effectively without a middle ear.

Assessing vocal performance in complex birdsong: a novel approach.

BACKGROUND: Vocal performance refers to the ability to produce vocal signals close to physical limits. Such motor skills can be used by conspecifics to assess a signaller's competitive potential. For example it is difficult for birds to produce repeated syllables both rapidly and with a broad frequency bandwidth. Deviation from an upper-bound regression of frequency bandwidth on trill rate has been widely used to assess vocal performance. This approach is, however, only applicable to simple trilled songs, and even then may be affected by differences in syllable complexity. RESULTS: Using skylarks (Alauda arvensis) as a birdsong model with a very complex song structure, we detected another performance trade-off: minimum gap duration between syllables was longer when the frequency ratio between the end of one syllable and the start of the next syllable (inter-syllable frequency shift) was large. This allowed us to apply a novel measure of vocal performance ¿ vocal gap deviation: the deviation from a lower-bound regression of gap duration on inter-syllable frequency shift. We show that skylarks increase vocal performance in an aggressive context suggesting that this trait might serve as a signal for competitive potential. CONCLUSIONS: We suggest using vocal gap deviation in future studies to assess vocal performance in songbird species with complex structure.

Amplitude modulation of sexy phrases is salient for song attractiveness in female canaries (Serinus canaria).

Song discrimination and recognition in songbird species have usually been studied by measuring responses to song playbacks. In female canaries, Serinus canaria, copulation solicitation displays (CSDs) are used as an index of female preferences, which are related to song recognition. Despite the fact that many studies underline the role of song syntax in this species, we observed that short segments of songs (a few seconds long) are enough for females to discriminate between conspecific and heterospecific songs, whereas such a short duration is not sufficient to identify the syntax rules. This suggests that other cues are salient for song recognition. In this experiment, we investigated the influence of amplitude modulation (AM) on the responses (CSDs) of female canaries to song playbacks. We used two groups of females: (1) raised in acoustic isolation and (2) raised in normal conditions. When adult, we tested their preferences for sexy phrases with different AMs. We broadcast three types of stimuli: (1) songs with natural canary AM, (2) songs with AM removed, or (3) song with wren Troglodytes troglodytes AM. Results indicate that female canaries prefer and have predispositions for a song type with the natural canary AM. Thus, this acoustic parameter is a salient cue for song attractiveness.

Acoustic communication in crocodilians: information encoding and species specificity of juvenile calls.

In the Crocodylia order, all species are known for their ability to produce sounds in several communication contexts. Though recent experimental studies have brought evidence of the important biological role of young crocodilian calls, especially at hatching time, the juvenile vocal repertoire still needs to be clarified in order to describe thoroughly the crocodilian acoustic communication channel. The goal of this study is to investigate the acoustic features (structure and information coding) in the contact call of juveniles from three different species (Nile crocodile Crocodylus niloticus, Black caiman, Melanosuchus niger and Spectacled caiman, Caiman crocodilus). We have shown that even though substantial structural differences exist between the calls of different species, they do not seem relevant for crocodilians. Indeed, juveniles and adults from the species studied use a similar and non-species-specific way of encoding information, which relies on frequency modulation parameters. Interestingly, using conditioning experiments, we demonstrated that this tolerance in responses to signals of different acoustic structures was unlikely to be related to a lack of discriminatory abilities. This result reinforced the idea that crocodilians have developed adaptations to use sounds efficiently for communication needs.

Are bird song complexity and song sharing shaped by habitat structure? An information theory and statistical approach.

In songbirds, song complexity and song sharing are features of prime importance for territorial defence and mate attraction. These aspects of song may be strongly influenced by changes in social environment caused by habitat fragmentation. We tested the hypothesis that habitat fragmentation induced by human activities influences song complexity and song sharing in the skylark, a songbird with a very large repertoire and whose population recently underwent a large decline. We applied powerful mathematical and statistical tools to assess and compare song complexity and song sharing patterns of syllables and sequences of syllables in two populations: a declining population in a fragmented habitat, in which breeding areas are separated from each other by unsuitable surroundings, and a stable population in a continuous habitat. Our results show that the structure of the habitat influences song sharing, but not song complexity. Neighbouring birds shared more syllables and sequences of syllables in the fragmented habitat than in the continuous one. Habitat fragmentation seems thus to have an effect on the composition of elements in songs, but not on the number and complexity of these elements, which may be a fixed feature of song peculiar to skylarks.

Mother-calf vocal communication in Atlantic walrus: a first field experimental study.

In all colonial pinnipeds studied, mother-young vocal recognition exists and allows rapid and reliable meetings in spite of the confusing environment of the breeding colony. The efficiency of this recognition process guarantees pup survival, especially in species where females alternate foraging sea trips and lactation periods on land. The Atlantic Walrus (Odobenus rosmarus rosmarus) is a highly gregarious pinniped with females attending their calves for an extended period of time (2-3 years). Although we expect mother-calf vocal recognition to occur in this species due to the high density of individuals packed in herds, it has never been experimentally demonstrated. Here, we assessed the individual stereotypy of both mother and calf barks recorded in the wild by measuring frequency and temporal acoustic parameters. Both discriminant function and artificial neural network analyses resulted in high correct classification rates, underlying a well-defined individual stereotypy in parameters related to frequency modulation and frequency values. Playback experiments showed that mothers were more responsive to the barks of their own calf than to those of unrelated young. Finally, propagation experiments revealed that barks propagate at greater distances over water surface than over ice, acoustic features such as frequency modulation and frequency spectrum being highly resistant to degradation during propagation. Thus, acoustic analysis and propagation experiments suggest that these frequency parameters might be the key acoustic features involved in the individual identification process. This experimental study clearly demonstrates that Atlantic walrus has developed a highly reliable mother-calf vocal communication allowing such strong social bond.

Influence of social conditions in song sharing in the adult canary.

In songbirds, experience of social and environmental cues during a discrete period after birth may dramatically influence song learning. In the canary, the ability to learn new songs is assumed to persist throughout life. The aim of the present study was to investigate whether social context could guide changes in adult song. Three groups of canaries were kept in different social and temporal conditions. Results showed that the multiple hierarchical levels of the canary song structure were affected by social environment: songs of males housed together for 2 years were more similar than those of males that spent the same time in individual cages in regard to acoustic parameters, syllable repertoire and repertoire of sequences of two-syllable types. However, social housing did not result in the emergence of a group-specific vocal signature within songs. In conclusion, these results suggested that under the influence of social factors, a copying process could allow adult canaries to adjust, at least in part, their songs to those of other individuals.

Response to displaced neighbours in a territorial songbird with a large repertoire.

Neighbour recognition allows territory owners to modulate their territorial response according to the threat posed by each neighbour and thus to reduce the costs associated with territorial defence. Individual acoustic recognition of neighbours has been shown in numerous bird species, but few of them had a large repertoire. Here, we tested individual vocal recognition in a songbird with a large repertoire, the skylark Alauda arvensis. We first examined the physical basis for recognition in the song, and we then experimentally tested recognition by playing back songs of adjacent neighbours and strangers. Males showed a lower territorial response to adjacent neighbours than to strangers when we broadcast songs from the shared boundary. However, when we broadcast songs from the opposite boundary, males showed a similar response to neighbours and strangers, indicating a spatial categorisation of adjacent neighbours' songs. Acoustic analyses revealed that males could potentially use the syntactical arrangement of syllables in sequences to identify the songs of their neighbours. Neighbour interactions in skylarks are thus subtle relationships that can be modulated according to the spatial position of each neighbour.

First evidence of underwater vocalisations in hunting penguins.

Seabirds are highly vocal on land where acoustic communication plays a crucial role in reproduction. Yet, seabirds spend most of their life at sea. They have developed a number of morphological, physiological and behavioural adaptations to forage in the marine environment. The use of acoustic signals at sea could potentially enhance seabirds' foraging success, but remains largely unexplored. Penguins emit vocalisations from the sea surface when commuting, a behaviour possibly associated with group formation at sea. Still, they are unique in their exceptional diving abilities and feed entirely underwater. Other air-breathing marine predators that feed under water, like cetaceans, pinnipeds and marine turtles, are known to emit sound underwater, but such behaviour has not yet been described in seabirds. We aimed to assess the potential prevalence and diversity of vocalisations emitted underwater by penguins. We chose three study species from three different genera, and equipped foraging adults with video cameras with built-in microphones. We recorded a total of 203 underwater vocalisation from all three species during 4 h 43 min of underwater footage. Vocalisations were very short in duration (0.06 s on average), with a frequency of maximum amplitude averaging 998 Hz, 1097 Hz and 680 Hz for King, Gentoo and Macaroni penguins, respectively. All vocalisations were emitted during feeding dives and more than 50% of them were directly associated with hunting behaviour, preceeded by an acceleration (by 2.2 s on average) and/or followed by a prey capture attempt (after 0.12 s on average). The function of these vocalisations remain speculative. Although it seems to be related to hunting behaviour, these novel observations warrant further investigation.

Snapshot recordings provide a first description of the acoustic signatures of deeper habitats adjacent to coral reefs of Moorea.

Acoustic recording has been recognized as a valuable tool for non-intrusive monitoring of the marine environment, complementing traditional visual surveys. Acoustic surveys conducted on coral ecosystems have so far been restricted to barrier reefs and to shallow depths (10-30 m). Since they may provide refuge for coral reef organisms, the monitoring of outer reef slopes and describing of the soundscapes of deeper environment could provide insights into the characteristics of different biotopes of coral ecosystems. In this study, the acoustic features of four different habitats, with different topographies and substrates, located at different depths from 10 to 100 m, were recorded during day-time on the outer reef slope of the north Coast of Moorea Island (French Polynesia). Barrier reefs appeared to be the noisiest habitats whereas the average sound levels at other habitats decreased with their distance from the reef and with increasing depth. However, sound levels were higher than expected by propagation models, supporting that these habitats possess their own sound sources. While reef sounds are known to attract marine larvae, sounds from deeper habitats may then also have a non-negligible attractive potential, coming into play before the reef itself.

Mate vocal recognition in the Scopoli's shearwater Calonectris diomedea: do females and males share the same acoustic code?

Vocal recognition is an important process allowing partners' reunion in most seabirds. Although the acoustic basis of this recognition has been explored in several species, only a few studies have experimentally tested the acoustic coding-decoding strategy used for mate identification. Here, we investigated mate recognition in the Scopoli's shearwater (Calonectris diomedea) by conducting playbacks of calls with modified acoustic features. We showed that females and males in a seabird species with a moderate vocal dimorphism are likely to share the same coding-decoding rule for vocal mate identification. Specifically, a disruption of call temporal structure prevented mate recognition in both sexes, in line with the parameters previously identified as supporting an individual signature. Modifications of spectral cues and envelope structure also impaired recognition, but at a lesser extent: almost half of the tested males and females were still able to recognise their partner. It is likely that this equal ability of female and male Scopoli's shearwaters to vocally recognise their partner could be found in other seabirds.

A study of vocal nonlinearities in humpback whale songs: from production mechanisms to acoustic analysis.

Although mammalian vocalizations are predominantly harmonically structured, they can exhibit an acoustic complexity with nonlinear vocal sounds, including deterministic chaos and frequency jumps. Such sounds are normative events in mammalian vocalizations, and can be directly traceable to the nonlinear nature of vocal-fold dynamics underlying typical mammalian sound production. In this study, we give qualitative descriptions and quantitative analyses of nonlinearities in the song repertoire of humpback whales from the Ste Marie channel (Madagascar) to provide more insight into the potential communication functions and underlying production mechanisms of these features. A low-dimensional biomechanical modeling of the whale's U-fold (vocal folds homolog) is used to relate specific vocal mechanisms to nonlinear vocal features. Recordings of living humpback whales were searched for occurrences of vocal nonlinearities (instabilities). Temporal distributions of nonlinearities were assessed within sound units, and between different songs. The anatomical production sources of vocal nonlinearities and the communication context of their occurrences in recordings are discussed. Our results show that vocal nonlinearities may be a communication strategy that conveys information about the whale's body size and physical fitness, and thus may be an important component of humpback whale songs.

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.

The two parts of the blackcap song: Acoustic analysis and male responses to playbacks.

Bird songs are complex manifold acoustic signals serving two main functions: mate attraction and territorial defense. The way information is encoded in the song often reflects adaptation to proximate and ultimate constraints. Male blackcaps, Sylvia atricapilla, display versatile songs with two parts, a warble and a whistle, whose functions remain unclear. We showed that the two parts of songs differ in terms of intensity, frequency and temporal parameters. They also contain totally different sets of syllables. Furthermore, the warble is versatile whereas the whistle part shows syllable sharing between individuals leaving closeby. Altogether, the results of our analysis suggest that the two parts encode different information potentially directed to different audiences. In order to test the potential function of these two parts, we performed playback experiments by broadcasting entire songs and each part separately. Warble and whistle alone are sufficient to trigger male responses and males sing both parts in responses to all stimuli, showing that both parts of the song are used in male-male competition. It is suggested that the segregation of information in the blackcap song could be related to public versus private communication, used in both intra- and intersexual contexts, rather than directed to male versus female audiences only.

Altered social behavior and ultrasonic communication in the dystrophin-deficient mdx mouse model of Duchenne muscular dystrophy.

BACKGROUND: The Duchenne and Becker muscular dystrophies (DMD, BMD) show significant comorbid diagnosis for autism, and the genomic sequences encoding the proteins responsible for these diseases, the dystrophin and associated proteins, have been proposed as new candidate risk loci for autism. Dystrophin is expressed not only in muscles but also in central inhibitory synapses in the cerebellum, hippocampus, amygdala, and cerebral cortex, where it contributes to the organization of autism-associated trans-synaptic neurexin-neuroligin complexes and to the clustering of synaptic gamma-aminobutyric acid (GABA)A receptors. While brain defects due to dystrophin loss are associated with deficits in cognitive and executive functions, communication skills and social behavior, only a subpopulation of DMD patients meet the criteria for autism, suggesting that mutations in the dystrophin gene may confer a vulnerability to autism. The loss of dystrophin in the mdx mouse model of DMD has been associated with cognitive and emotional alterations, but social behavior and communication abilities have never been studied in this model. METHODS: Here, we carried out the first in-depth analysis of social behavior and ultrasonic communication in dystrophin-deficient mdx mice, using a range of socially relevant paradigms involving various degrees of executive and cognitive demands, from simple presentation of sexual olfactory stimuli to social choice situations and direct encounters with female and male mice of various genotypes. RESULTS: We identified context-specific alterations in social behavior and ultrasonic vocal communication in mdx mice during direct encounters in novel environments. Social behavior disturbances depended on intruders' genotype and behavior, suggesting alterations in executive functions and adaptive behaviors, and were associated with selective alterations of the development, rate, acoustic properties, and use of the ultrasonic vocal repertoire. CONCLUSIONS: This first evidence that a mutation impeding expression of brain dystrophin affects social behavior and communication sheds new light on critical cognitive, emotional, and conative factors contributing to the development of autistic-like traits in this disease model.

How a songbird with a continuous singing style modulates its song when territorially challenged.

In songbirds of the temperate zone, often only males sing and their songs serve to attract females and to deter territorial rivals. In many species, males vary certain aspects of their singing behavior when engaged in territorial interactions. Such variation may be an honest signal of the traits of the signaler, such as fighting strength, condition, or aggressive motivation, and may be used by receivers in decisions on whether to retreat or to escalate a fight. This has been studied intensively in species that sing discontinuously, in which songs are alternating with silent pauses. We studied contextual variation in the song of skylarks (Alauda arvensis), a songbird with a large vocal repertoire and a continuous and versatile singing style. We exposed subjects to simulated territorial intrusions by broadcasting conspecific song and recorded their vocal responses. We found that males sing differently if they are singing spontaneously with no other conspecific around than if they are territorially challenged. In this last case, males produced lower-frequency syllables. Furthermore, they increased the sound density of their song: they increased the proportion of sound within song. They seem to do so by singing different elements of their repertoire when singing reactively. Furthermore, they increased the consistency of mean peak frequency: they repeated syllable types with less variability when singing reactively. Such contextual variation suggests that skylarks might use low frequencies, sound density, and song consistency to indicate their competitive potential, and thus, those song features might be important for mutual assessment of competitive abilities.

Flight phases in the song of skylarks: impact on acoustic parameters and coding strategy.

Skylarks inhabit open fields and perform an aerial song display which serves as a territorial signal. The particularly long and elaborate structure of this song flight raises questions about the impact of physical and energetic constraints acting on a communication signal. Song produced during the three distinct phases of the flight - ascending, level and descending phase could be subject to different constraints, serve different functions and encode different types of information. We compared song parameters during the ascending and the level phases. We found that the structure of the song varied with the phase of the flight. In particular, song had a higher tempo when skylarks were ascending which might be related to higher oxygen and energetic demands. We also explored which phase of the song flight might encode individuality. Earlier studies reported that skylarks reduced their territorial response to established neighbours if the neighbour song was broadcasted from the correct adjacent boundary, but reacted aggressively if the neighbour songs were broadcasted from an incorrect boundary (mimicking a displaced neighbour). Such differential response provides some evidence for individual recognition. Here, we exposed subjects to playback stimuli of neighbour song in which we had replaced either the song produced during the level or the ascending phase by the relevant song of the neighbour from the incorrect border. Singing response was higher towards stimuli in which the 'level phase song' was replaced, indicating that skylarks could be able to recognise their neighbours based on song of this phase. Thus, individuality seems to be primarily coded in the level phase of the flight song.

Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment.

Social interactions in mice are frequently analysed in genetically modified strains in order to get insight of disorders affecting social interactions such as autism spectrum disorders. Different types of social interactions have been described, mostly between females and pups, and between adult males and females. However, we recently showed that social interactions between adult males could also encompass cognitive and motivational features. During social interactions, rodents emit ultrasonic vocalizations (USVs), but it remains unknown if call types are differently used depending of the context and if they are correlated with motivational state. Here, we recorded the calls of adult C57BL/6J male mice in various behavioral conditions, such as social interaction, novelty exploration and restraint stress. We introduced a modulator for the motivational state by comparing males maintained in isolation and males maintained in groups before the experiments. Male mice uttered USVs in all social and non-social situations, and even in a stressful restraint context. They nevertheless emitted the most important number of calls with the largest diversity of call types in social interactions, particularly when showing a high motivation for social contact. For mice maintained in social isolation, the number of calls recorded was positively correlated with the duration of social contacts, and most calls were uttered during contacts between the two mice. This correlation was not observed in mice maintained in groups. These results open the way for a deeper understanding and characterization of acoustic signals associated with social interactions. They can also help evaluating the role of motivational states in the emission of acoustic signals.