Song parameters of the fuscous honeyeater Lichenostomus fuscus correlate with habitat characteristics in fragmented landscapes

Both avian abundance and species richness decline in response to habitat loss and fragmentation. Studying variation in bird song structure across modified landscapes can provide insights into the effects of habitat alterations on coherence of social interactions within populations. Here, we tested whether fragmentation or change of habitat quality within box‐ironbark forest of central Victoria impacted cultural connectivity and song characteristics in fuscous honeyeater, a declining common Australian bird. First, we tested whether geographic distance and/or spatially‐explicit landscape connectivity models can explain patterns of song similarity across fragmented landscapes. We found no evidence that distance or habitat fragmentation impacts the nature and transmission of fuscous honeyeater song, and concluded that acoustic connectivity at the scale of our study is high. Second, we tested whether variation in habitat quality explains variation in song characteristics. In accordance with acoustic adaptation to habitat structure, birds sang longer songs in sites with more large trees and produced longer common song elements in sites with greater tree height. However, the acoustic adaptation hypothesis cannot explain the finding that in less‐disturbed landscapes with higher tree‐cover birds sang songs (and song elements) with higher maximum frequency and wider frequency bandwidth. We also found that birds sing longer and more variable songs of wider frequency bandwidth in less disturbed sites with a greater number of large mature trees, which may represent better feeding resources. Our study suggests that changes in song structure with habitat degradation could signal disturbed population processess, such as changes in the acoustic communication among resident birds.     

Body size correlates negatively with the frequency of distress calls and songs of Neotropical birds

ABSTRACT The allometric relationship between body size and song frequency has been established in previous studies of temperate and tropical bird communities. However, the relationship between body size and the frequency of distress calls has been examined in only one study of temperate birds. We examined size‐frequency relationships in the distress calls and songs of a Neotropical bird community in northwestern Costa Rica. In 2008 and 2009, we recorded distress calls and determined the body mass of 54 mist‐netted birds representing 38 species, 35 genera, and 14 families. We obtained songs for these same species from sound libraries and commercially available compact discs. For each vocalization, we measured minimum frequency and frequency of maximum amplitude. Larger birds produced lower‐frequency distress calls and songs than smaller birds. Phylogenetically controlled analyses revealed that the frequency of maximum amplitude was negatively correlated with body mass for both distress calls and songs. Minimum frequency was negatively correlated with mass for distress calls, but not songs. Our analyses suggest that the influence of phylogeny on the relationship between frequency characteristics and body size is modest. Pair‐wise comparisons across 37 species revealed that distress calls and songs had similar minimum frequencies, but songs had significantly lower frequencies of maximum amplitude than distress calls. This difference may arise from differences in signal function. Lower‐frequency sounds should transmit farther through forest habitats and songs must often transmit longer distances to reach their intended audience than distress calls. Our results support the general theory that body size is negatively correlated with the frequency of acoustic signals by demonstrating that this pattern holds true for both distress calls and songs in a Neotropical bird community.     

Sexually size dimorphic brains and song complexity in passerine birds

Neural correlates of bird song involve the volume of particularsong nuclei in the brain that govern song development, production,and perception. Intra- and interspecific variation in the volumeof these song nuclei are associated with overall brain size,suggesting that the integration of complex songs into the brainrequires general neural augmentation. In a comparative studyof passerine birds based on generalized least square models,we tested this hypothesis by exploring the interspecific relationshipbetween overall brain size and repertoire size. We found nosignificant association between song complexity of males andbrain size adjusted for body size. However, species in whichmales produced complex songs tended to have sex differencesin overall brain size. This pattern became stronger when wecontrolled statistically for female song complexity by usingsex differences in song complexity. In species with large differencesin song complexity, females evolved smaller brains than didmales. Our results suggest no role for the evolution of extendedneural space, as reflected by total brain size, owing to songcomplexity. However, factors associated with sexual selectionmirrored by sex differences in song complexity were relatedto sexual dimorphism in overall brain size.     

The learning advantage: bird species that learn their song show a tighter adjustment of song to noisy environments than those that do not learn

Song learning has evolved within several avian groups. Although its evolutionary advantage is not clear, it has been proposed that song learning may be advantageous in allowing birds to adapt their songs to the local acoustic environment. To test this hypothesis, we analysed patterns of song adjustment to noisy environments and explored their possible link to song learning. Bird vocalizations can be masked by low‐frequency noise, and birds respond to this by singing higher‐pitched songs. Most reports of this strategy involve oscines, a group of birds with learning‐based song variability, and it is doubtful whether species that lack song learning (e.g. suboscines) can adjust their songs to noisy environments. We address this question by comparing the degree of song adjustment to noise in a large sample of oscines (17 populations, 14 species) and suboscines (11 populations, 7 species), recorded in Brazil (Manaus, Brasilia and Curitiba) and Mexico City. We found a significantly stronger association between minimum song frequency and noise levels (effect size) in oscines than in suboscines, suggesting a tighter match in oscines between song transmission capacity and ambient acoustics. Suboscines may be more vulnerable to acoustic pollution than oscines and thus less capable of colonizing cities or acoustically novel habitats. Additionally, we found that species whose song frequency was more divergent between populations showed tighter noise–song frequency associations. Our results suggest that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution of song learning and plasticity.     

Differences in Frequency of Shared Song Types Enables Neighbour‐Stranger Discrimination in a Songbird Species with Small Song Repertoire

Acoustic Neighbour‐Stranger (N‐S) discrimination is widespread in birds and has evolved to settle territorial disputes with low costs. N‐S discrimination was found both in song‐learning oscines and non‐song‐learning bird taxa, irrespective of the repertoire sizes they have. Therefore, it seems that more than just a single mechanism enable N‐S discrimination. Species with larger repertoires, where males have unique phrases or syllables may rely on such interindividual differences. The majority of birds have rather small repertoires, which often are shared among neighbours. In this case, males are facing the problem of individual recognition when rivals produce songs, at least superficially, identical. To better understand the acoustic basis of N‐S discrimination in species with small and shared repertoires, I studied the ortolan bunting (Emberiza hortulana). Males of this small oscine species are able to N‐S discrimination based on a single song rendition when presented in a playback experiment, regardless of song‐type diversity and song‐sharing level within a particular population. It was also found that songs of the same type sung by different males differ in the frequency of the initial song phrases and these differences persist over years. Here, I tested whether males are able to discriminate among the natural songs and the artificially modified songs of their neighbours in which the frequency was experimentally changed by relatively small value in comparison with the variation range found in this population. Subjects responded significantly more aggressively to the songs with an artificially modified frequency, suggesting that males treat such songs as having come from the repertoire of a non‐neighbour. These results confirm an earlier prediction that differences in the frequency of shared song types enable N‐S discrimination. The study presents one of the possible mechanisms enabling N‐S discrimination in songbirds with small repertoires and stress the role of within‐song‐type variation, which is still understudied song characteristic.     

Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.     

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.     

Recent northward range expansion promotes song evolution in a passerine bird,the Light‐vented Bulbul

In common with human speech, song is culturally inherited in oscine passerine birds (‘songbirds’). Intraspecific divergence in birdsong, such as development of local dialects, might be an important early step in the speciation process. It is therefore vital to understand how songs diverge, especially in founding populations. The northward expansion of the Light‐vented Bulbul Pycnonotus sinensis (J. F. Gmelin, 1789) into north China in the last 30 years provides an excellent opportunity to study birdsong evolution. We compared ~4400 songs from newly established northern populations with ~2900 songs from southern populations to evaluate song divergence after recent expansion. The total pool of syllables and especially song types was considerably smaller in the north than in the south, indicating ‘founder effects’ in the new population. The ancestral pattern of mosaic song dialects changed into a pattern of wide geographical sharing of a few song types and syllables, likely the result of fewer geographical barriers to ‘meme flow’, and the recent spread across a large area in the north. Our results suggest that song evolution and vocal trait shifts can arise rapidly after range expansion, and that in the Light‐vented Bulbul ‘founder effects’, geographical isolation, and recent rapid expansions played important roles in the evolution of song dialects.     

Black‐capped chickadees Poecile atricapillus sing at higher pitches with elevated anthropogenic noise,but not with decreasing canopy cover

Several songbird species sing at higher frequencies (i.e. higher pitch) when anthropogenic noise levels are elevated. Such frequency shifting is thought to be an adaptation to prevent masking of bird song by anthropogenic noise. However, no study of this phenomenon has examined how vegetative differences between noisy and quiet sites influence frequency shifting. Variation in vegetative structure is important because the acoustic adaptation hypothesis predicts that birds in more open areas should also sing at higher frequencies. Thus, vegetative structure may partially explain the observation of higher frequency songs in areas with high levels of anthropogenic noise. To distinguish between frequency shifting due to noise or vegetative structure we recorded the songs of black‐capped chickadees Poecile atricapillus vocalizing in high and low noise sites with open and closed canopy forests. Consistent with the noise‐dependent frequency hypothesis, black‐capped chickadees sang at higher frequencies in high noise sites than in low noise sites. In contrast, birds did not sing at higher frequencies in sites with more open canopies. These results suggest that frequency shifting in chickadees is more strongly related to ambient noise levels than to vegetative structure. A second frequency measure, inter‐note ratio, was reduced at higher levels of canopy cover. We speculate that this may be due to a non‐random distribution of dominant males. In sum, our results support the hypothesis that some birds sing at higher frequencies to avoid overlap with anthropogenic noise, but suggest that vegetative structure may play a role in the modification of other song traits.     

A hierarchical neuronal model for generation and online recognition of birdsongs

The neuronal system underlying learning, generation and recognition of song in birds is one of the best-studied systems in the neurosciences. Here, we use these experimental findings to derive a neurobiologically plausible, dynamic, hierarchical model of birdsong generation and transform it into a functional model of birdsong recognition. The generation model consists of neuronal rate models and includes critical anatomical components like the premotor song-control nucleus HVC (proper name), the premotor nucleus RA (robust nucleus of the arcopallium), and a model of the syringeal and respiratory organs. We use Bayesian inference of this dynamical system to derive a possible mechanism for how birds can efficiently and robustly recognize the songs of their conspecifics in an online fashion. Our results indicate that the specific way birdsong is generated enables a listening bird to robustly and rapidly perceive embedded information at multiple time scales of a song. The resulting mechanism can be useful for investigating the functional roles of auditory recognition areas and providing predictions for future birdsong experiments.     

The evolution of birdsong on islands

Islands are simplified, isolated ecosystems, providing an ideal set‐up to study evolution. Among several traits that are expected to change on islands, an interesting but poorly understood example concerns signals used in animal communication. Islands are typified by reduced species diversity, increased population density, and reduced mate competition, all of which could affect communication signals. We used birdsong to investigate whether there are systematic changes in communication signals on islands, by undertaking a broad comparison based on pairs of closely related island‐mainland species across the globe. We studied song traits related to complexity (number of different syllables, frequency bandwidth), to vocal performance (syllable delivery rate, song duration), and also three particular song elements (rattles, buzzes, and trills) generally implicated in aggressive communication. We also investigated whether song complexity was related to the number of similar sympatric species. We found that island species were less likely to produce broadband and likely aggressive song elements (rattles and buzzes). By contrast, various aspects of song complexity and performance did not differ between island and mainland species. Species with fewer same‐family sympatric species used wider frequency bandwidths, as predicted by the character release hypothesis, both on continents and on islands. Our study supports the hypothesis of a reduction in aggressive behavior on islands and suggests that discrimination against closely related species is an important factor influencing birdsong evolution.     

Evolution of leaf warbler songs (Aves: Phylloscopidae)

Songs in passerine birds are important for territory defense and mating. Speciation rates in oscine passerines are so high, due to cultural evolution, that this bird lineage makes up half of the extant bird species. Leaf warblers are a speciose Old‐World passerine family of limited morphological differentiation, so that songs are even more important for species delimitation. We took 16 sonographic traits from song recordings of 80 leaf warbler taxa and correlated them with 15 potentially explanatory variables, pairwise, and in linear models. Based on a well‐resolved molecular phylogeny of the same taxa, all pairwise correlations were corrected for relatedness with phylogenetically independent contrasts and phylogenetic generalized linear models were used. We found a phylogenetic signal for most song traits, but a strong one only for the duration of the longest and of the shortest element, which are presumably inherited instead of learned. Body size of a leaf warbler species is a constraint on song frequencies independent of phylogeny. At least in this study, habitat density had only marginal impact on song features, which even disappeared through phylogenetic correction. Maybe most leaf warblers avoid the deterioration through sound propagation in dense vegetation by singing from exposed perches. Latitudinal (and longitudinal) extension of the breeding ranges was correlated with most song features, especially verse duration (longer polewards and westwards) and complexity (lower polewards). Climate niche or expansion history might explain these correlations. The number of different element types per verse decreases with elevation, possibly due to fewer resources and congeneric species at higher elevations.     

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.     

Rock sparrow song reflects male age and reproductive success

The evolution of mating signals is closely linked to sexual selection. Acoustic ornaments are often used as secondary sexual traits that signal the quality of the signaller. Here we show that song performance reflects age and reproductive success in the rock sparrow (Petronia petronia). In an Alpine population in south-east France, we recorded the songs of males and assessed their genetic breeding success by microsatellite analysis. In addition to temporal and spectral song features, we also analysed for the first time whether the sound pressure level of bird song reflects reproductive success. Males with higher breeding success sang at a lower rate and with a higher maximum frequency. We found also that older males gained more extra-pair young and had a higher overall breeding success, although they also differed almost significantly by having a higher loss of paternity in their own nests. Older males could be distinguished from yearlings by singing at lower rate and higher amplitudes. Our findings suggest that song rate may be used as a signal of age and together with song pitch as a signal of reproductive success in this species. Alternatively, younger and less successful males might try to compensate their inferior status by increased song rates and lower pitch. Independent of age and quality, high-amplitude songs correlated with paternity loss in the own nest, suggesting that in this species song amplitude is not an indicator of male quality but high-intensity songs may be rather a response to unfaithful social mates.     

Age‐dependent song changes in a closed‐ended vocal learner: elevation of song performance after song crystallization

Birdsong is a sexual signal that serves as an indicator of male quality. There is already abundant evidence that song elaboration reflects early life‐history because early developmental stress affects neural development of song control systems, and leaves irreversible adverse effects on song phenotypes. Especially in closed‐ended vocal learners, song features crystallized early in life are less subject to changes in adulthood. This is why less attention has been paid to lifelong song changes in closed‐ended learners. However, in the eyes of female birds that gain benefits from choosing mates based on male songs, not only past but also current conditions encoded in songs would be meaningful, given that even crystallized songs in closed‐ended learners would not be identical in the long term. In this study, we examine within‐individual song changes in the Java sparrow Lonchura oryzivora, with the aim of shedding light on the relationship between song and long‐term life history. Specifically, we compared song length, tempo, and song complexity measures between the point just after song crystallization and around 1 yr later, and also compared those traits between fathers and sons to clarify the effect of vocal learning. While it is not surprising that song complexity did not differ depending on age or between fathers and sons, we found that song length and tempo increased with age. Follow‐up analyses have revealed that frequency bandwidth and peak frequency of song notes also elevated with age. Our results show that song performance related to motor skills can be improved even after song crystallization. We also suggest that song performance in closed‐ended vocal learners gives a reliable clue for mate choice by reflecting male quality with aging.     

Repertoire Sharing and Song Similarity between Great Tit Males Decline with Distance between Forest Fragments

Birdsong can play a critical role in establishing a territory and finding a mate among individuals from local and foreign populations. Variation in birdsong among populations can be influenced by habitat fragmentation and might affect successful dispersal among habitat fragments. We studied variation in great tit song in a long‐term study population distributed over nine forest fragments. All individual males recorded had a known dispersal history within the fragmented forest habitat. We found spatial structure of declining song‐type sharing with distance, with a marked drop from an individual’s own forest fragment to another across a habitat gap. We also found decreasing song similarity among increasingly distant fragments in terms of temporal and spectral characteristics of shared song types. The change in acoustic structure was more gradual and seemed less affected by habitat discontinuity but also showed a tight correlation with dispersal index among forest fragments. Immigrant birds shared fewer song types with neighbouring birds that were born within the same forest fragment, but not less compared to birds born in another forest fragment within the study area. Our data provide detailed insight into the relationship between song differentiation and male dispersal and contribute to our understanding of the potential role of song in reproductive exchange and avian speciation. The fact that birds in small forest fragments shared more songs than birds in larger forest fragments confirms that song analysis has potential as a tool for conservation in rare species.     

Captive Rearing Experiments Confirm Song Development without Learning in a Tracheophone Suboscine Bird

The origin of vocal learning in animals has long been the subject of debate, but progress has been limited by uncertainty regarding the distribution of learning mechanisms across the tree of life, even for model systems such as birdsong. In particular, the importance of learning is well known in oscine songbirds, but disputed in suboscines. Members of this diverse group (∼1150 species) are generally assumed not to learn their songs, but empirical evidence is scarce, with previous studies restricted to the bronchophone (non-tracheophone) clade. Here, we conduct the first experimental study of song development in a tracheophone suboscine bird by rearing spotted antbird (Hylophylax naevioides) chicks in soundproofed aviaries. Individuals were raised either in silence with no tutor or exposed to standardized playback of a heterospecific tutor. All individuals surviving to maturity took a minimum of 79 days to produce a crystallized version of adult song, which in all cases was indistinguishable from wild song types of their own species. These first insights into song development in tracheophone suboscines suggest that adult songs are innate rather than learnt. Given that empirical evidence for song learning in suboscines is restricted to polygamous and lek-mating species, whereas tracheophone suboscines are mainly monogamous with long-term social bonds, our results are consistent with the view that sexual selection promotes song learning in birds.     

Male and female rufous‐and‐white wrens do not match song types with same‐sex rivals during simulated territorial intrusions

In birds with song repertoires, song‐type matching occurs when an individual responds to another individual's song by producing the same song type. Song‐type matching has been described in multiple bird species and a growing body of evidence suggests that song‐type matching may serve as a conventional signal of aggression, particularly in male birds in the temperate zone. Few studies have investigated song‐type matching in tropical birds or female birds, in spite of the fact that avian biodiversity is highest in the tropics, that female song is widespread in the tropics, and that female song is the ancestral state among songbirds. In this study of rufous‐and‐white wrens Thryophilus rufalbus, a resident neotropical songbird where both sexes sing, we presented territorial males and females with playback that simulated a territorial rival producing shared and unshared songs. In response, both males and females sang matched song types at levels statistically equal to levels expected by chance. Furthermore, males and females exhibited similar levels of aggression and similar vocal behaviours in response to playback of both shared and unshared songs. These results indicate that rufous‐and‐white wrens do not use song‐type matching in territorial conflicts as a conventional signal of aggression. We discuss alternative hypotheses for the function of song‐type sharing in tropical birds. In particular, we point out that shared songs may play an important role in intra‐pair communication, especially for birds where males and females combine their songs in vocal duets, and this may supersede the function of song‐type matching in some tropical birds.     

Non‐Salient Geographic Variation in Birdsong in a Species That Learns by Improvisation

Geographic variation in birdsong and differential responses of territorial males to local and non‐local song variants have been documented in a number of songbird species in which males learn their songs through imitation. Here, we investigated geographic song variation and responses to local and non‐local song in the grasshopper sparrow (Ammodramus savannarum), a species in which males develop song by improvisation rather than imitation, as a first step toward understanding how the extent and salience of geographic song variation is related to the mode of song development. To describe the geographic variation in song, we compared songs from populations in eastern Maryland and central Ohio, USA, using multiple acoustic analysis techniques. We then conducted a playback experiment in Maryland using local and non‐local (Ohio) songs to test how territorial males responded to this geographic variation. We found acoustic differences between songs from the two sites. However, males responded similarly to playback of these songs, suggesting that this geographic variation is not behaviorally salient in a territorial context. Together with previous studies, our results suggest that across species, geographic song variation and the extent to which this variation functions in communication may be correlated with the accuracy with which song models are imitated during song development.     

Songbirds learn songs least degraded by environmental transmission

Communication depends on accurate reception of signals by receivers, and selection acts on signals to transmit efficiently through the environment. Although learnt signals, such as birdsong, vary in their transmission properties through different habitats, few studies have addressed the role of cultural selection in driving acoustic adaptation. Here, we present a test of the hypothesis that song-learning birds choose to copy songs that are less degraded by transmission through the environment, using swamp sparrows (Melospiza georgiana) as our study species. We found that all subjects discriminated between undegraded and naturally degraded song models, and learnt only from undegraded song models, demonstrating a role for cultural selection in acoustic adaptation of learnt signals.