MICRODIALECT AND GROUP SIGNATURE IN THE SONG OF THE SKYLARK ALAUDA ARVENSIS

ABSTRACT

The Skylark Alauda arvensis is a territorial species of open landscape in which pairs settle in stable and adjacent territories during the breeding season. Due to the heterogeneity of the habitat, territories are gathered in patches spaced by a few kilometres, in which each male produces very long and complex flight songs as a part of the territorial behaviour. We showed that, in a given patch, all the males (neighbours) share some particular sequences of syllables in their songs, whereas males settled in different patches (strangers) have almost no sequences in common. Such a phenomenon is known as microdialect. To test the hypothesis that these shared sequences support a group signature, we made playback experiments with “chimeric” signals: songs of strangers where the sequences shared by neighbours were artificially inserted. Behavioural responses to playbacks indicated a neighbour-stranger discrimination consistent with the dear enemy phenomenon, i.e. a reduced aggression toward neighbours compared to strangers. Furthermore, the same level of responses, observed when a “chimeric” song and a neighbour song were broadcast, indicated that shared sequences are recognised and identified as markers of the neighbourhood identity.     

Seasonal and diel plasticity of song type use in individual ovenbirds (Seiurus aurocapilla)

Animal communication is an important aspect of ecology across taxa, and there is a growing area of research that examines how animals plastically adjust their signals to account for both abiotic and biotic factors. Song type use and the temporal plasticity of song have been described in many bird species, but as of yet, few studies have examined how song type use may change across both seasonal and diel timeframes, and no studies have considered individual-level variation in plasticity. Using a hierarchical framework, we examined temporal patterns of primary and flight song use in ovenbirds (Seiurus aurocapilla; N = 21 individuals). We recorded ovenbird songs (N = 99,259) with autonomous recorders over 24-hr periods once per week across a breeding season near Sault Ste. Marie, Canada. As predicted, the occurrence and frequency of both song types significantly decreased over the season and showed temporal separation over diel periods. Primary songs peaked at dawn and declined throughout the day, while flight songs peaked at dusk and night. Our results support that primary songs have multiple functions as they remained more frequent during dawn and morning across the breeding season, while flight songs likely serve an intersexual function as they decreased similarly for all diel periods as mating opportunities decreased. Individuals were consistent in how frequently they sang their primary songs, but not their flight songs, suggesting that flight songs are more plastically expressed. We highlight the importance of examining plasticity in animal communication at the individual level as we show that males significantly differed in both their song behaviours (random intercepts) and the seasonal plasticity (random slopes) in these behaviours. Integrating themes such as song type use, temporal plasticity, and individual variation will be important for examining the evolutionary mechanisms that shape animal communication systems.     

Song Types and their Use: Developmental Flexibility of the Male Blue-winged Warbler

How does an animal know the appropriate context in which to use its different vocalizations? I studied this problem with a songbird, the blue-winged warbler (Vermivora pinus). Mated males in nature tend to sing one song form (II) at dawn, under low light levels, and at a median rate of 15 songs/min. Their other song (I, the more familiar bee-buzz) is used later in the day, under higher light levels, and at a median rate of 6 songs/min. In the laboratory I tutored different groups of hand-reared males under normal circumstances (group 1: song II early in the morning, under low light, at a rapid rate; song I later, under high light, at a slow rate), under reversed circumstances (group 2: song I early, low light, rapid rate; etc.), and with no contextual cues (group 3: songs I and II both early and late, under both light levels, and at an intermediate rate). Few males developed entirely normal blue-wing song, but males of group 2 clearly reversed the use of song forms and components. The relationship between signal form and function in the songs of this warbler appears flexible and to some extent learned by the males.     

The Influence of Song Mode on Responses of Male American Redstarts

Male American redstarts (Setophaga ruticilla) exhibit two modes of singing: repeat and serial mode. Repeat mode consists of repetitions of a single song type, usually one possessing an accented terminal note. Serial mode is constituted by a series of different songs with unaccented terminal notes, sung in a versatile sequence. Different authors have observed that males discriminate between these two modes. In the experiments reported in this paper, we tested whether males use accented terminal notes, song versatility or both to discriminate between the two song modes. We observed that males responded more intensively to the accented song. The accented note seems a very important song characteristic for evoking male American redstart responses. In contrast, males did not show any difference in their response to single and varied serial songs.     

Song modification in the Orthoptera I. Proclamation songs of Platycleis spp. (Tettigoniidae)

Orthopteran song terminology is briefly reviewed taking into account new proposals concerning the term ‘chirp’ by Broughton (1976). The song of Platycleis intermedia is analysed in detail. Synchronous or unison singing between conspecifics of this species is maintained, despite ambient temperature differences, by the individual at the lower temperature instantaneously extending its echeme interval. The normal songs of P.afinis, P.falx, P.sabulosa and P.albopunctata are described and compared with each other and with the song of P.intermedia. The songs of all five species are similar at the syllable level but different at the echeme level. It appears to be these similarities and differences that are responsible for song modification on the part of P.intermedia when it hears the song of one of the other four species.     

Effects of location in territory and distance from neighbours on the use of song repertoires by Carolina wrens

By capturing territorial Carolina wrens (Thryothorus ludovicianus) and housing them in portable cages on their territories, I could control each one's location in its territory and distance from neighbours in experiments on the use of song repertoires. Experiment 1 demonstrated that these wrens sang more songs in the centre of their territories than at the edge, but that they did not use more song types or different song types at the centre than at the edge. In experiment 2, in which I played tape-recorded songs at two distances from wrens caged in the centres of their territories, birds responded more strongly to songs at 25m, simulating an intruder, than to songs at 165 m, simulating a territorial neighbour. Birds also switched more frequently between song types and sang more song types per 100 songs in response to the nearer playback. Experiment 3 compared captive wrens 140 m, 80 m, 20 m, or 0 m apart on adjacent territories. As the distance between neighbours decreased, birds sang less, but also switched more frequently between song types, used more song types per 100 songs, and matched songs with neighbours more frequently. There were no differences in the kinds of song types sung at different distances from neighbours. A comparison of the results from experiments 1 and 3 confirms that the use of song repertoires is influenced by distance from conspecifics and not by location in the territory.     

Rock wrens preferentially use song types that improve long distance signal transmission during natural singing bouts

When animals are capable of producing variable signals they may preferentially use some signal types over others. Among songbirds, individuals are known to alter song type form and usage patterns in contest and mating situations, but studies have not examined how song choice improves signal efficacy during broadcast song. For this study we investigated rock wren Salpinctes obsoletus song type use rates during natural singing bouts. We tested three hypotheses for adaptive song use during broadcast song: 1) birds improve signal content by increasing the use of high quality songs, 2) birds optimize for signal propagation by preferentially using songs that transmit well, and 3) birds maintain energy by reducing the use of costly songs. The study included 19 058 songs sung by 12 individuals, each of which had a measured song repertoire of between 52 and 117 song types which were produced at highly variable rates. Results indicated that rock wrens did not preferentially sing song types with shorter durations or fewer frequency switches, as would be expected if they selected song types to minimize delivery costs. They also did not favor songs with more rapid trills or more frequency switches, as would be expected if they adjusted song use primarily to indicate quality. Focal birds did preferentially sing significantly longer songs with lower bandwidths, lower frequencies, and slower trill rates. Results suggest that natural broadcast singing patterns are shaped more by the benefits of long distance transmission than by the benefits of advertising performance ability or the costs of song production.     

An Interactive Playback Experiment Shows Song Bout Size Discrimination in the Suboscine Vermilion Flycatcher (Pyrocephalus rubinus)

Many aspects of the social behaviour of birds are mediated by vocal displays, and variation in song output or song structure conveys different information to receivers. After nest construction begins, when vermilion flycatcher (Pyrocephalus rubinus) females are potentially fertile, males increase their song rate during the dawn chorus. A previous study failed to give evidence that males discriminate among song rates. However, males sing in sequences of songs (song bouts), and an increase in song rate may be achieved by increasing the number of bouts, the number of songs in each bout (bout size) or both. Studying a vermilion flycatcher population in Mexico City, we evaluated whether dawn song rate is related to song bout size or to number of bouts. Bout size correlated with song rate and differed among males. We hypothesized that longer bouts are more threatening signals than shorter ones and predicted a stronger response by males towards the former. We exposed each male to three playback treatments: (1) Long song bout (Long), in which we replied to the male with twice the number of songs he sang in the bout, (2) Short song bout (Short), in which we played half the number of songs sung by the male and (3) Control, this was the same as the Long treatment but we used songs from a related species, the tropical kingbird (Tyrannus melancholicus). Males responded with a higher proportion of calls near the speaker when exposed to the Long treatment than during the Short or Control treatments, indicating that they discriminate among song bouts differing in size, that they may perceive longer bouts as more threatening and that they use calls rather than songs to address threatening situations. Our results suggest that song bout size is a relevant song attribute that conveys information during intrasexual interactions.     

Acoustic mate copying: female cowbirds attend to other females' vocalizations to modify their song preferences

We conducted a tutoring experiment to determine whether female brown-headed cowbirds (Molothrus ater) would attend to vocalizations of other females and use those cues to influence their own preferences for male courtship songs. We collected recordings of male songs that were unfamiliar to the subject females and paired half of the songs with female chatter vocalizations—vocalizations that females give in response to songs sung by males that are courting the females effectively. Thus, chatter immediately following a song provided a cue indicating that the song was sung by a male who was of high-enough quality to court a female successfully. Using a cross-over design, we tutored two groups of females with song–chatter pairings prior to the breeding season. In the breeding season, we placed the tutored females into sound-attenuating chambers and played them the same songs without the chatter. Females produced significantly more copulation solicitation displays in response to the songs that they had heard paired with chatter than to songs that had not been paired with chatter. This experiment is the first demonstration that females can modify their song preferences by attending to the vocal behaviour of other females.     

Song organisation and patterns of variation in the serin (Serinus serinus)

This article describes the organisation of song in the serin (Serinus serinus) and analyses its variation among individuals. Serins have a repertoire of about 50 complex syllables that are sung at a very fast rate and in a very stereotyped order, forming discrete songs. Songs are high pitched for the serin’s body size. Song organisation is circular, with a limited number of starting points. Songs can stop at any point in their cycling. Within songs there are trilled sections and fast, non-repeated sections that account for the greatest part of songs. These two modes of singing also differ in average inter-element intervals and probably in their respiratory kinematics. Bird repertoire size was measured and the difficulties of measuring it in this species are discussed. Repertoires are individually specific and have a variable amount of syllable sharing with other birds. We found evidence for geographical variation in the composition of repertoires. Considering our current knowledge of song in carduelines, the stereotyped and circular nature of serin song appear to be unique within this group of birds. Received: 30 May 2000 / Received in revised from: 14 August 2000 / Accepted: 12 September 2000     

Acoustic signals in insects: A reproductive barrier and a taxonomic character

In singing insects, the song is an important component of the specific mate recognition system (SMRS). In communities of sympatric singing species, there is a partitioning of communication channels, the so-called “acoustic niches.” Within one community, the songs of different species always differ in temporal or frequency characters, i.e. occupy different acoustic niches. However, conspecific songs do not always act as an interspecific reproductive barrier, despite always being a SMRS component. The species that do not communicate acoustically due to allopatry, different timing of vocalization, inhabiting different biotopes, or unmatched food specializations can produce similar songs while forming reproductively isolated communities. Individuals of different sexes need not only to recognize a conspecific mate but also to evaluate its “quality.” The close-range signal (courtship song) provides more opportunities for choosing the “best” male than does the distant signal (calling song). In many species of Orthoptera, courtship includes not only acoustic but also vibrational, visual, chemical, and mechanical signals. An analysis of cricket songs showed the courtship songs to be on average more elaborate and variable than the calling songs. At the same time, due to the difference in mating behavior between the two groups, the acoustic component of courtship is used for mate quality evaluation to a greater extent in grasshoppers than in crickets. The courtship songs of grasshoppers are generally more elaborate in temporal structure than cricket songs; moreover, they may be accompanied by visual displays such as movements of various body parts. Thus, song evolution in grasshoppers is more strongly driven by sexual selection than that in crickets. According to the reinforcement hypothesis, the premating barrier between hybridizing species becomes stronger in response to reduced hybrid fitness. However, our behavioral experiments with two groups of hybridizing grasshopper species did not confirm the reinforcement hypothesis. We explain this, firstly, by a low level of genetic incompatibility between the hybridizing species and secondly, by high hybrid fitness when attracting a mate. A high competitive capability of hybrids may be accounted for by attractiveness of new elements in hybrid courtship songs. When we divide similar forms based on their songs, we in fact distinguish biological species using the criterion of their reproductive isolation. Acoustic differences between species are usually greater than morphological ones. Therefore, song analysis allows one to determine the real status of doubtful species-rank taxa, to distinguish species in a medley of sibling forms, and to reveal cryptic species in the cases when morphological studies fail to provide a univocal result. At the same time, songs are subject to intraspecific variation the range of which is different in different groups. Therefore, it is necessary to study which degree of difference corresponds to the species level before interpreting the status of some forms based on song comparisons. Besides, song similarities cannot indicate conspecificity of acoustically isolated forms; on the other hand, song differences between these forms prove that they are full-rank species.     

The song structure and seasonal patterns of vocal behavior of male and female bellbirds (Anthornis melanura)

The bellbird (Anthornis melanura) is a honeyeater endemic to New Zealand, which uses song to defend breeding territories and/or food resources year round. Both sexes sing and the song structure and singing behavior have not yet been quantified. The number of song types, spectral structure, repertoire size, and singing behavior of male and female bellbirds was investigated for a large island population. Song types differed between the sexes with males singing a number of structurally distinct song types and females producing song types that overlapped in structure. Singing behavior also differed between the sexes; males often sung long series of songs while females sung each song at relatively long and variable intervals. Singing by both sexes occurred year round but the frequency of male and female singing bouts showed contrasting seasonal patterns. The frequency of female singing bouts increased as the breeding season progressed, whereas male singing bouts decreased. In contrast to almost all studied passerines, female bellbirds exhibited significant singing behavior and sung songs of complex structure and variety that parallel male song. These results provide a quantitative foundation for further research of song in bellbirds and in particular the function of female vocal behavior.     

Causes of the latitudinal gradient in birdsong complexity assessed from geographical variation within two Himalayan warbler species

Aspects of birdsong complexity, such as the number of distinct notes in a song, commonly increase along latitudinal gradients, a pattern for which at least 10 explanations have been suggested. In two Himalayan warblers, songs are more complex in the northwest than in the southeast. In Grey‐hooded Warbler Phylloscopus xanthoschistos, high complexity results from increased note diversity within song types, sung across a higher bandwidth. In Blyth's Leaf Warbler Phylloscopus reguloides, high complexity is a consequence of increased variation between song types. The hypothesis with strongest support is that songs evolved to be more complex in species‐poor, demonstrably less noisy environments. We consider geographical variation to be an outcome of sexual selection favouring complexity across environments, where detection of the signal varies. Sexual selection favouring complexity may be resolved in different ways, because complexity has multiple features (repertoire size, song switching, etc.). We argue this has led to the great diversity in song that we have documented among five Phylloscopus species.     

Advertising vocalization of the clamorous reed warbler (<Emphasis Type="Italic">Acrocephalus stentoreus</Emphasis>, Sylviidae)

The advertising vocalization of the clamorous reed warbler, one of the least studied representatives of the genus in the Palearctic, has been analyzed. In this species, advertising vocalization consists of compact acoustic constructs (songs) separated by pauses. The duration of songs (median 3.6 s) and pauses (median 2.9 s) varies only slightly. Each song consists of three to four different or identical syllables. Syllables (stereotyped acoustic constructs) consist of two to four notes. Each male has from 5 to 25 syllables in his repertoire. A sharp contrast between low-frequency and high-frequency notes and strict sequence of these notes in syllables (low-frequency notes come first, then follow high-frequency notes) are characteristic of this song. All types of syllables in the song of a given male can be divided into two groups: initiator syllables and other syllables. Initiator syllables most often occur at the beginning, while others occur in the middle or at the end of the song. Stable links between syllables have been revealed: the majority of them occur in the song together with certain syllables (one or two) of other types. The whole range of songs of each individual can be divided into several classes. A certain type of initiator syllable and a certain set of subsequent syllables are characteristic of each class. However, the variability of songs within each class is quite high. Modes of immediate and eventual variety alternate in the sequence of songs from different classes. Thus, 47.4% of songs are followed by a song from the same class (eventual variety), while 52.6% of songs are followed by a song from a different class (immediate variety). The advertising vocalization of the clamorous reed warbler is compared with that of other representatives of the genus Acrocephalus.     

Soft Song in Song Sparrows: Acoustic Structure and Implications for Signal Function

In many species of songbirds, males sometimes produce songs at distinctly lower amplitude than in normal singing. Depending on the species, these 'soft songs' may be sung in the context of female courtship, male–male aggression, or both. In song sparrows, males produce soft songs during aggressive interactions with other males, and the amount of soft song produced is the only singing behavior that can be used to reliably predict a subsequent attack by the singer. Although soft song is clearly an important signal in this species, little is known about the acoustic structure of soft song or about how that structure compares to the structure of normal 'broadcast song'. We recorded a large sample of soft songs and broadcast songs from 10 male song sparrows, and measured song amplitudes in the field while controlling the subject's distance to a calibrated microphone. We show that song sparrow males produce songs over a wide range of amplitudes, with soft songs in the range of 55–77 dB sound pressure level and broadcast songs in the range of 78–85 dB. We present evidence for two types of soft song: 'crystallized' soft songs that are broadcast repertoire song types sung at low amplitude, and 'warbled' soft songs that are not found in the broadcast repertoire. Although highly variable, warbled soft songs produced by individual birds could be grouped into song types based on spectrographic similarity. To our knowledge, a distinct repertoire of soft song types has not been previously reported for any songbird.     

Courtship song analysis of Drosophila muscle mutants

As part of the mating ritual, males of Drosophila species produce species-specific courtship songs through wing vibrations generated by the thoracic musculature. While previous studies have shown that indirect flight muscles (IFM) are neurally activated during courtship song production, the precise role of these muscles in song production has not been investigated. Fortunately, IFM mutants abound in Drosophila melanogaster and studies spanning several decades have shed light on the role of muscle proteins in IFM-powered flight. Analysis of courtship songs in these mutants offers the opportunity to uncover the role of the IFM in a behavior distinct than flight and subject to different evolutionary selection regimes. Here, we describe protocols for the recording and analysis of courtship behavior and mating song of D. melanogaster muscle transgenic and mutant strains. To record faint acoustic signal of courtship songs, an insulated mating compartment was used inside a recording device (INSECTAVOX) equipped with a modified electret microphone, a low-noise power supply, and noise filters. Songs recorded in the INSECTAVOX are digitized using Goldwave, whose several features enable extraction of critical song parameters, including carrier frequencies for pulse song and sine song. We demonstrate the utility of this approach by showing that deletion of the N-terminal region of the myosin regulatory light chain, a mutation known to decrease wing beat frequency and flight power, affects courtship song parameters.     

Individual Distinctiveness and Possible Function of Song Parts of Short-toed Treecreepers (Certhia brachydactyla). Evidence from Multivariate Song Analysis

Sonagram analyses of short-toed treecreeper (= STT) song by use of discriminant analysis revealed consistent individuality in the songs predominantly sung by each male (P-songs). The P-songs had been digitized and over 30 song variables were used in the analysis to separate different individuals. In the end, 7 of these variables were needed for a correct classification of 100% of the 203 P-songs recorded of 39 individuals in 1986. Most of these variables were derived from the first part of the song. A similar analysis with data from 1987 showed that by use of all variables with unskewed distribution complete discrimination of all 271 P-songs of 47 individuals ensued. The reduction of variables to the 10 most important led to the correct classifications of 99.5%. Using the 7 best discriminators of the 1986 data set 94.2% of the 1987 data were correctly classified, thus confirming the 1986 results. Wrong assignments were mainly due to P-songs from second or third recording dates which in some cases could not be separated from other P-songs of the same males by the analysis. Further analysis of the data showed that although the most important discriminators were found in the first part of the song, the combination of all characters of the end part would also allow for a virtually complete discrimination of individuals. The song features of STT P-song are so distinctive that territory holders should have no difficulties in separating individuals (e.g. neighbours from strangers). Corresponding playback experiments have yet to be carried out on STT.     

Manipulations of sensory experiences during development reveal mechanisms underlying vocal learning biases in zebra finches

Biological predispositions in learning can bias and constrain the cultural evolution of social and communicative behaviors (e.g., speech and birdsong), and lead to the emergence of behavioral and cultural “universals.” For example, surveys of laboratory and wild populations of zebra finches (Taeniopygia guttata) document consistent patterning of vocal elements (“syllables”) with respect to their acoustic properties (e.g., duration, mean frequency). Furthermore, such universal patterns are also produced by birds that are experimentally tutored with songs containing randomly sequenced syllables (“tutored birds”). Despite extensive demonstrations of learning biases, much remains to be uncovered about the nature of biological predispositions that bias song learning and production in songbirds. Here, we examined the degree to which “innate” auditory templates and/or biases in vocal motor production contribute to vocal learning biases and production in zebra finches. Such contributions can be revealed by examining acoustic patterns in the songs of birds raised without sensory exposure to song (“untutored birds”) or of birds that are unable to hear from early in development (“early‐deafened birds”). We observed that untutored zebra finches and early‐deafened zebra finches produce songs with positional variation in some acoustic features (e.g., mean frequency) that resemble universal patterns observed in tutored birds. Similar to tutored birds, early‐deafened birds also produced song motifs with alternation in acoustic features across adjacent syllables. That universal acoustic patterns are observed in the songs of both untutored and early‐deafened birds highlights the contribution motor production biases to the emergence of universals in culturally transmitted behaviors.