Booming far: the long-range vocal strategy of a lekking bird.

The pressures of selection acting on transmission of information by acoustic signals are particularly high in long-distance communication networks. Males of the North African houbara bustard (Chlamydotis undulata undulata) produce extremely low-frequency vocalizations called 'booms' as a component of their courtship displays. These displays are performed on sites separated by a distance of on average 550 m, constituting exploded leks. Here, we investigate the acoustic features of booms involved in species-specific identity. We first assessed the modifications of acoustic parameters during boom transmission at long range within the natural habitat of the species, finding that the frequency content of booms was reliably transmitted up to 600 m. Additionally, by testing males' behavioural responses to playbacks of modified signals, we found that the presence of the second harmonic and the frequency modulation are the key parameters for species identification, and also that a sequence of booms elicited stronger responses than a single boom. Thus, the coding-decoding process relies on redundant and propagation-resistant features, making the booms particularly well adapted for the long-range transmission of information between males. Moreover, by experimentally disentangling the presentation of visual and acoustic signals, we showed that during the booming phase of courtship, the two sensory modalities act in synergy. The acoustic component is dominant in the context of intra-sexual competition. While the visual component is not necessary to induce agonistic response, it acts as an amplifier and reduces the time of detection of the signaller. The utilization of these adaptive strategies allows houbara males to maximize the active space of vocalizations emitted in exploded leks.

Size does matter: crocodile mothers react more to the voice of smaller offspring.

Parental care is widespread in Archosaurs (birds, crocodilians, dinosaurs and pterosaurs), and this group provides a useful model for the evolution of parent-offspring interactions. While offspring signalling has been well-studied in birds, the modulation of parental care in crocodilians remains an open question. Here we show that acoustic communication has a key role in the dynamics of crocodilian' mother-offspring relationships. We found embedded information about the emitter's size in juvenile calls of several species, and experimentally demonstrated that Nile crocodile mothers breeding in the wild are less receptive to the calls of larger juveniles. Using synthetized sounds, we further showed that female' reaction depends on call pitch, an important cue bearing size information. Changes in acoustic interactions may thus go with the break of maternal care as well as dispersal of juvenile crocodilians. This process could have characterized other archosaurs displaying rapid early growth such as dinosaurs and pterosaurs.

Is microhabitat segregation between two cicada species (Tibicina haematodes and Cicada orni) due to calling song propagation constraints?

The cicada species Tibicina haematodes and Cicada orni are two sympatric species often inhabiting vineyards. We show that they occupy two distinct levels: males of T. haematodes produce their calling songs from a high position in vine foliage while males of C. orni call from a low position near the ground on vine trunks. Experiments consisting of broadcasting and re-recording experimental signals in natural habitats from low and high positions show that signals are more and more modified as sender-receiver distance increases. T. haematodes would have an advantage when calling on trunks rather than on branches whereas C. orni would be able to call indiscriminately from both low and high positions. Thus, the microhabitat segregation observed between T. haematodes and C orni in vineyards does not seem to be related to calling song propagation constraints, but may be due to other ethological or ecological factors.

Functional coupling of acoustic and chemical signals in the courtship behaviour of the male Drosophila melanogaster.

During courtship, the male Drosophila melanogaster sends signals to the female through two major sensory channels: chemical and acoustic. These signals are involved in the stimulation of the female to accept copulation. In order to determine the respective importance in the courtship of these signals, their production was controlled using genetical and surgical techniques. Males deprived of the ability to emit both signals are unable to mate, demonstrating that other (e.g. visual or tactile) signals are not sufficient to stimulate the female. If either acoustic or chemical signals are lacking, the courtship success is strongly reduced, the lack of the former having significantly more drastic effects. However, the accelerated matings of males observed with males bearing wild-type hydrocarbons compared with defective ones, whichever the modality of acoustic performance (wing vibration or playback), strongly support the role of cuticular compounds to stimulate females. We can conclude that among the possible factors involved in communication during courtship, acoustic and chemical signals may act in a synergistic way and not separately in D. melanogaster.

Compared ontogenesis of courtship song components of males from the sibling species, D. melanogaster and D. simulans.

The courtship song of Drosophila is known to be an important signal involved in sex and species recognition. It consists of pulse song and sine song, which have been studied in a quantitative way with different parameters. For the first time the setting of both components of the acoustic signaling is described and compared for males belonging to the sibling species D. melanogaster and D. simulans. At early ages, these two species share similar interpulse interval values but maturation establishes the species specificity of this character. For D. melanogaster the variations of several acoustic parameters take place in two successive periods, whereas for D. simulans the majority of the acoustic features does not change much with age. In D. melanogaster, copulation success seems to be linked to the maturation of the acoustic performance, which is not the case for D. simulans.

The rally call recognition in males of two hybridizing partridge species, red-legged (Alectoris rufa) and rock (A. graeca) partridges.

The red-legged (Alectoris rufa) and rock (A. graeca) partridges hybridize and produce fertile offspring along a contact zone in French Southern Alps. The rally call emitted during pair formation, could play an important role in species recognition, acting as a behavioral reproductive isolating mechanism between males and females. In the present study, the coding system of the rally call was investigated from captive males of the two species and from F1 hybrids. By playing-back natural signals, we found that the two species as well as hybrid males responded to Alectoris signals but not to another species belonging to the Phasianidae family (Colinus virginianus). Results also indicate that red-legged and rock partridges responded stronger to conspecific calls than to heterospecific ones. However, they reacted similarly to conspecific and hybrid calls. F1 hybrids responded stronger to hybrids calls than to the two species ones. They did not distinguish the two parental species signals from each other. Although the two species showed the ability to discriminate the conspecific from the heterospecific signal, they clearly responded to the other species. This behaviour may play a role in the hybridization phenomenon.

Intra-syllabic acoustic signatures used by the king penguin in parent-chick recognition: an experimental approach.

In king penguin colonies, several studies have shown that both parent-chick recognition and mate-pair recognition are achieved by acoustic signals. The call of king penguins consists of strong frequency modulations with added beats of varying amplitude induced by the two-voice generating process. Both the frequency modulation pattern and the two-voice system could play a role in the identification of the calling bird. We investigated the potential role of these features in individual discrimination. Experiments were conducted by playing back altered or reconstructed parental signals to the corresponding chick. The results proved that the king penguin performs a complex analysis of the call, using both frequency modulation and the two-voice system. Reversed or frequency-modulation-suppressed signals do not elicit any responses. Modifying the shape of the frequency modulation by 30 % also impairs the recognition process. Moreover, we have demonstrated for the first time that birds perform an analysis of the beat amplitude induced by the two-voice system to assess individual identity. These two features, which are well preserved during the propagation of the signal, seem to be a reliable strategy to ensure the accurate transmission of individual information in a noisy colonial environment.

Penguins use the two-voice system to recognize each other.

The sound-producing structure in birds is the syrinx, which is usually a two-part organ located at the junction of the bronchi. As each branch of the syrinx produces sound independently, many birds have two acoustic sources. Thirty years ago, we had anatomical, physiological and acoustical evidence of this two-voice phenomenon but no function was known. In songbirds, often these two voices with their respective harmonics are not activated simultaneously but they are obvious in large penguins and generate a beat pattern which varies between individuals. The emperor penguin breeds during the Antarctic winter, incubating and carrying its egg on its feet. Without the topographical cue of a nest, birds identify each other only by vocal means when switching duties during incubation or chick rearing. To test whether the two-voice system contains the identity code, we played back the modified call of their mate to both adults and also the modified call of their parents to chicks. Both the adults and the chicks replied to controls (two voices) but not to modified signals (one voice being experimentally suppressed). Our experiments demonstrate that the beat generated by the interaction of these two fundamental frequencies conveys information about individual identity and also propagates well through obstacles, being robust to sound degradation through the medium of bodies in a penguin colony. The two-voice structure is also clear in the call of other birds such as the king penguin, another non-nesting species, but not in the 14 other nesting penguins. We concluded that the two-voice phenomenon functions as an individual recognition system in species using few if any landmarks to meet. In penguins, this coding process, increasing the call complexity and resisting sound degradation, has evolved in parallel with the loss of territoriality.

Perceptual salience of individually distinctive features in the calls of adult king penguins.

In the king penguin, Aptenodytes patagonicus, incubation and brooding duties are undertaken alternately by both partners of a pair. Birds returning from foraging at sea find their mate in the crowded colony using acoustic signals. Acoustic recognition of the mate maintains and strengthens the mate's fidelity and favors synchronization in the different stages of reproduction. In this study it was found that the king penguin vocalizes in response to the mate's playback calls, but not to those of neighbors or unfamiliar conspecific individuals. To study individual features used by the birds for individual recognition of mates, various experimental signals consisting of synthesized modifications of the mate' s call were played back to the incubating bird. Results indicated that birds attend to the FM profile of the call, in particular its initial inflexion. The frequency modulation shape of the syllable can be assimilated to a vocal signature repeated though the different syllables of the call. King penguins pay little attention to the call' s AM envelope or its absolute frequency.

Finding a parent in a king penguin colony: the acoustic system of individual recognition.

To be fed, a king penguin, Aptenodytes patagonicus, chick must identify the call of its parents, in the continuous background noise of the colony. To study this recognition process, we played back to the chicks parental calls with acoustic parameters modified in the temporal and frequency domains. The parental call is composed of syllables (complex sounds with harmonic series) separated by pronounced amplitude declines. Our experiments with modified signals indicate that the chick's frequency analysis of the call is not tuned towards precise peak energy values, the signal being recognized even when the carrier frequency was shifted 100 Hz down or 75 Hz up. To recognize the adult, chicks used frequency rather than amplitude modulation, in particular the frequency modulation shape of the syllable. This structure is repeated through the different syllables of the call giving a distinct vocal signature. Our experiments also show that the receiver needs to perceive only a small part of the signal: the first half of the syllable (0.23 s) and the first three harmonics were sufficient to elicit recognition. The small amount of information necessary to understand the message, the high redundancy in the time and frequency domains and the almost infinite possibilities of coding provided by the frequency modulation signature permit the chick to recognize the adult, without the help of a nest site. For these reasons, the code used in the call of the king penguin can be regarded as a functional code, increasing the possibility of individual recognition in an acoustically constraining environment. Copyright 1999 The Association for the Study of Animal Behaviour.

Propagation of bird acoustic signals: comparative study of starling and blackbird distress calls.

Previous works have demonstrated that the information supported by a bird distress call is encoded both by the energy distribution among harmonics and the temporal evolution of the frequency modulation. In the present study, using these parameters, we compared long-range information transfer in a dense vegetation environment between the starling Sturnus vulgaris and the blackbird. Turdus merula distress calls. It appears that excess attenuation of high frequencies (higher than 4 kHz) after a long-range propagation is responsible for modifications in distress call spectra. The energy of propagated signals tends to be concentrated in a 1.5-4-kHz bandwidth whatever the initial spectrum. Owing to its broad spectrum (0.8-7 kHz), the starling distress call is greatly modified. On the contrary, owing to a narrower spectrum (2-5.5 kHz), the blackbird distress call is relatively preserved. The blackbird distress call appears to be well-adapted to long-range transmission in an environment with dense vegetation. In contrast, the starling distress call is far more easily degraded by propagation. Nevertheless, frequency modulation of the starling call is preserved and message decoding remains possible even if message reliability may diminish. This result is examined from an etho-ecological point of view, taking into account both habitat and social structure of both birds.

Reaction to conspecific degraded song by the wren Troglodytes troglodytes: Territorial response and choice of song post.

We investigated the response of the wren Troglodytes troglodytes to playback of a territorial song degraded by long-range propagation. It appears that the wren is sensitive to this degradation since the territorial reaction is less intense with the degraded song than with the undegraded one. However, the degraded song is still considered by the receiver as a specific territorial aggressive signal. This differential response suggests that the male wren can use the degradation characteristics of the signal to adapt its territorial reaction. Indeed, in response to this stimulus, the receiver wren chooses a higher song post. By so doing, the bird improves both the propagation distance of the emitted song and the receiver's ability to hear the opponent's song. This behavioural change may correspond to a communication strategy, counteracting the environmental constraints on sound propagation. Therefore, in response to sound degradation during long-range propagation, birds may have developed behavioural adaptations complementary to the various adaptations concerning song structure and coding-decoding processes.

Why do distress calls evoke interspecific responses? An experimental study applied to some species of birds.

Distress calls of birds are well-known to elicit interspecific responses when they are broadcast to different species. We suggest that the interspecificity phenomenon results from the use of similar laws of decoding by all species. To support this hypothesis, we broadcast a simplified synthetic call to five species of birds (Larus argentatus, L. ridibundus, Vanellus vanellus, Corvus frugilegus and Sturnus vulgaris). This synthetic call was built by keeping all the parameters involved in the process of recognition and common to the different species and by removing species specific markers. No significant differences were found between this signal and specific control signals (one for each species). These results support the hypothesis that the interspecificity of responses is linked to similarities in the process of identification of the distress message. In addition, the decoding law of such calls appears to conform to selection pressures imposed by physical laws of sound transmission at long range.