Song Complexity Research Articles

The structure and context of male and female song in White-throated Dippers

Female song in birds is more widespread than previously thought but remains poorly studied. Relatively few researchers have compared the structure and function of female song with that of conspecific males, especially in non-duetting species. Here we investigate male and female song in the White-throated Dipper (Cinclus cinclus; hereafter ‘Dipper’), a highly territorial and largely monogamous passerine with a complex song in both sexes. The songs of individually marked birds were recorded over a 3-year period in order to compare the acoustic structure and production of song in males and females at different stages of the breeding cycle. No differences were found in the complexity, frequency or temporal characteristics of male and female songs. However, unpaired males recorded early in the breeding season sang more complex songs than males that were paired up and nest-building or whose breeding attempts were underway, suggesting that male song is used for mate attraction. By contrast, females sang most often during aggressive encounters with birds from outside their territory. Furthermore, males sang throughout the breeding season, when they are highly territorial, whereas females rarely sang after laying had begun. Together, these results support findings from other species that song structure varies with context and suggest that female song in Dippers may be used primarily in mate or territory defence.

Prenatal exposure to incubation calls affects song learning in the zebra finch

Songbirds are important models for understanding the mechanisms and fitness consequences of imitative vocal learning. Although the effects of early-life environmental and social conditions on song learning are well-established, the impact of early sound exposure has received surprisingly little attention. Yet recent evidence hints at auditory sensitivity in songbird embryos, including in the zebra finch (Taeniopygia guttata), a classic model species for song learning. Here, we tested whether prenatal exposure to incubation calls—highly rhythmic parental vocalisations produced on the nest—affected song learning in zebra finches. Embryos were exposed in the egg to either incubation (treatment) or contact (control) calls, and after hatching were reared in a large colony. The playback treatment did not affect song complexity nor the accuracy of song copying from the social father, but instead increased learning of non-paternal song syllables. This, in turn, improved males’ mounting success in mating trials. These effects may be attributable to changes in juvenile social behaviours, as playback also influenced male behaviour during mating trials. Our study provides the first experimental evidence that prenatal acoustic environment affects song learning and courtship behaviour in songbirds, thereby raising interesting questions on the role of innate versus acquired biases for vocal learning.

Influence of early-life nutritional stress on songbird memory formation.

In birds, vocal learning enables the production of sexually selected complex songs, dialects and song copy matching. But stressful conditions during development have been shown to affect song production and complexity, mediated by changes in neural development. However, to date, no studies have tested whether early-life stress affects the neural processes underlying vocal learning, in contrast to song production. Here, we hypothesized that developmental stress alters auditory memory formation and neural processing of song stimuli. We experimentally stressed male nestling zebra finches and, in two separate experiments, tested their neural responses to song playbacks as adults, using either immediate early gene (IEG) expression or electrophysiological response. Once adult, nutritionally stressed males exhibited a reduced response to tutor song playback, as demonstrated by reduced expressions of two IEGs (Arc and ZENK) and reduced neuronal response, in both the caudomedial nidopallium (NCM) and mesopallium (CMM). Furthermore, nutritionally stressed males also showed impaired neuronal memory for novel songs heard in adulthood. These findings demonstrate, for the first time, that developmental conditions affect auditory memories that subserve vocal learning. Although the fitness consequences of such memory impairments remain to be determined, this study highlights the lasting impact early-life experiences can have on cognitive abilities.

Description of the song of the Nilgiri Thrush (Zoothera [aurea] neilgherriensis) and song differentiation across the Zoothera dauma species complex

BackgroundTaxonomic treatment of the Zoothera dauma species complex is highly variable and has been hampered by the absence of song recordings for the Nilgiri Thrush (Zoothera [aurea] neilgherriensis).MethodsI obtained two recordings of the song of neigherriensis from southern Indian. Here I publish sonograms and analyze song recordings for all but one currently described taxon from the Eurasian portion of the geographic range of this species complex. Principal component analyses were used to investigate song differences between taxa.ResultsThe song of neigherriensis is a highly complex series of strophes remarkably similar to the song of the insular Zoothera major. Vocal analyses across the complex indicate four key groups of taxa differentiated in their songs: (1) simple flat whistled songs which include the northern aurea, toratugumi and the undescribed Taiwan population; (2) eastern populations of dauma (reported here for the first time) which sing like northern birds but with much broader bandwidth, (3) strongly down-slurred, thin whistles of tropical resident imbricata of Sri Lanka and horsfieldi of Indonesia, and (4) highly complex songs of Himalayan dauma, neilgherriensis and major.ConclusionsZoothera dauma is unlikely to represent a single species given the simple singing populations from its eastern range and highly complex song from the Himalayan portion of its range. neilgherriensis should either be transferred from Zoothera aurea, where it is currently classified as a subspecies, and be placed as a subspecies within Z. dauma from the Himalayas or it should be recognized as a distinct species. Given the small number of songs available for analyses, I suggest the former course until it can be clearly demonstrated that neilgherriensis and Himalayan dauma are vocally distinct.

The relationship between latitude, migration and the evolution of bird song complexity

For the past several decades it has been proposed that birds show latitudinal variation in song complexity. How universal this variation may be and what factors generate it, however, are still largely unknown. Furthermore, while migration is confounded with latitude, migratory behaviour alone may also be associated with variation in song complexity. In this paper we review the literature to assess current ideas on how latitude and migratory behaviour may drive large‐scale geographical patterns of song complexity. At least seven distinct hypotheses have been proposed in 29 studies of the topic. Four of these hypotheses posit that sexual selection pressures co‐vary with latitude and/or migration, resulting in concordant changes in song. Other hypotheses suggest that mechanisms other than sexual selection, such as large‐scale changes in environmental sound transmission properties, may be at play. Sixteen studies found support for increased song complexity with increased latitude and/or migration, whereas 13 did not. Relatively few studies exist on this topic, and methodological differences between them and variable definitions of ‘complexity’ make it difficult to determine whether results are comparable and concordant. At a minimum, it is possible to conclude there is no strong evidence that song complexity increases with latitude and/or migration in all birds. Future work should focus on examining multiple hypotheses at once to further advance our understanding of how latitude, migration and song complexity may or may not be related.

Male song diversity and its relation to breeding success in southern house wrensTroglodytes aedon chilensis

Theory proposes an adaptive relationship between male song complexity, including large song repertoires, and improved breeding success. Evidence supporting these relationships exists but is sometimes mixed or weak. Here we provide a first comprehensive study of the relationship between male song diversity and breeding success in a non‐migratory, austral population of house wrensTroglodytes aedon chilensisbreeding in Mendoza, Argentina. During a two‐year field study, we measured breeding success for a population of 62 males and recorded more than 34 000 songs from a subsample of 26 males. For the latter subsample, we tested for correlations between six measures of song diversity and four canonical measures of annual breeding success. Males that sang with greater overall syllable type diversity and that had larger song repertories paired with females that bred earlier and laid more eggs over the course of the breeding season. However, these males also showed lower levels of immediate song type diversity, as measured by the Levenshtein distance between successive songs. We discuss implications for the evolution of song complexity in this exceptionally widespread species and the selective mechanisms that might influence song complexity in resident populations in the Neotropics compared to migratory populations in the northern hemisphere.

MHC-mediated sexual selection on birdsong: Generic polymorphism, particular alleles and acoustic signals.

Several hypotheses predict that the major histocompatibility complex (MHC) drives mating preference in females. Olfactory, colour or morphological traits are often found as reliable signals of the MHC profile, but the role of avian song mediating MHC-based female choice remains largely unexplored. We investigated the relationship between several MHC and acoustic features in the collared flycatcher (Ficedula albicollis), a European passerine with complex songs. We screened a fragment of the class IIB second exon of the MHC molecule, of which individuals harbour 4-15 alleles, while considerable sequence diversity is maintained at the population level. To make statistical inferences from a large number of comparisons, we adopted both null-hypothesis testing and effect size framework in combination with randomization procedures. After controlling for potential confounding factors, neither MHC allelic diversity nor the presence of particular alleles was associated remarkably with the investigated qualitative and quantitative song traits. Furthermore, genetic similarity among males based on MHC sequences was not reflected by the similarity in their song based on syllable content. Overall, these results suggest that the relationship between features of song and the allelic composition and diversity of MHC is not strong in the studied species. However, a biologically motivated analysis revealed that individuals that harbour an MHC allele that impairs survival perform songs with broader frequency range. This finding suggests that certain aspects of the song may bear reliable information concerning the MHC profile of the individuals, which can be used by females to optimize mate choice.

Developmental changes in song production in free-living male and female New Zealand bellbirds

Song development research has been dominated by studies of northern hemisphere species where typically only males sing. However, female song is present in many species and recent research shows that female song is in fact the ancestral trait for songbirds. Here we present results from a field-based cross-sectional study comparing song development in both sexes of New Zealand bellbirds, Anthornis melanura. We asked whether both sexes develop song at a similar rate, and how the components of a song differ with age. The motor phases of each sex began at similar ages, with subsong starting at 3 weeks posthatching and song types crystallizing by 24 weeks. Song components were compared between three age groups: learning phase, first breeding season and adults. Song structure and acoustic properties were similar between sexes within the learning phase (except for mean fundamental frequency) but differed in adults. The variety of syllable types produced was more widespread in the learning phase and differed significantly between age groups and sexes. Individual syllable production varied in consistency between age groups for both sexes and we suggest that more complex syllables may require more practice to develop to maturity. The findings support the consensus that female and male bellbirds learn song at similar rates; however, differences between the sexes in the learned song components result in sexually dimorphic songs. This study is novel in that we used a field-based approach in which the complex song of male and female wild birds was compared between age groups ranging from fledging to adulthood. Our study contributes to current knowledge of female song development, a topic important for further understanding the selection pressures driving song evolution in songbirds.

Song recorded near a super-group of humpback whales on a mid-latitude feeding ground off South Africa.

Humpback whales (Megaptera novaeangliae) are well known for their complex song which is culturally transmitted and produced by males. However, the function of singing behavior remains poorly understood. Song was observed from 57 min of acoustic recording in the presence of feeding humpback whales aggregated in the near-shore waters on the west coast of South Africa. The structural organization of the song components, lack of overlap between song units, and consistency in relative received level suggest the song was produced by one "singer." The unusual timing and location of song production adds further evidence of plasticity in song production.

Extreme diversity in the songs of Spitsbergen's bowhead whales.

Almost all mammals communicate using sound, but few species produce complex songs. Two baleen whales sing complex songs that change annually, though only the humpback whale (Megaptera novaeangliae) has received much research attention. This study focuses on the other baleen whale singer, the bowhead whale (Balaena mysticetus). Members of the Spitsbergen bowhead whale population produced 184 different song types over a 3-year period, based on duty-cycled recordings from a site in Fram Strait in the northeast Atlantic. Distinct song types were recorded over short periods, lasting at most some months. This song diversity could be the result of population expansion, or immigration of animals from other populations that are no longer isolated from each other by heavy sea ice. However, this explanation does not account for the within season and annual shifting of song types. Other possible explanations for the extraordinary diversity in songs could be that it results either from weak selection pressure for interspecific identification or for maintenance of song characteristics or, alternatively, from strong pressure for novelty in a small population.

Global macroevolution and macroecology of passerine song.

Studying the macroevolution of the songs of Passeriformes (perching birds) has proved challenging. The complexity of the task stems not just from the macroevolutionary and macroecological challenge of modeling so many species, but also from the difficulty in collecting and quantifying birdsong itself. Using machine learning techniques, we extracted songs from a large citizen science dataset, and then analyzed the evolution, and biotic and abiotic predictors of variation in birdsong across 578 passerine species. Contrary to expectations, we found few links between life-history traits (monogamy and sexual dimorphism) and the evolution of song pitch (peak frequency) or song complexity (standard deviation of frequency). However, we found significant support for morphological constraints on birdsong, as reflected in a negative correlation between bird size and song pitch. We also found that broad-scale biogeographical and climate factors such as net primary productivity, temperature, and regional species richness were significantly associated with both the evolution and present-day distribution of bird song features. Our analysis integrates comparative and spatial modeling with newly developed data cleaning and curation tools, and suggests that evolutionary history, morphology, and present-day ecological processes shape the distribution of song diversity in these charismatic and important birds.

An analysis of white-handed gibbon male song reveals speech-like phrases.

Our goal was to document song phrases of the white-handed gibbon (Hylobates lar), an Asian ape that produces elaborate songs, often in well-coordinated male/female duets. We focused on the male coda, which is produced during vocal turn-taking with one's mate, and particularly its phrases containing rapid spectral and temporal variation, to investigate if modulation rates resemble those of lip-smacking in other nonhuman primates and human speech rhythm. We produced recordings from a large population of wild gibbons. Using terminology consistent with that used to describe vocalizations in other singing species, we analyzed coda phrases, overall coda properties, coda distinctiveness across individuals, and flexibility of phrase production within song bouts. Our song phrase-level analysis showed that male codas differed between individuals and increase in complexity within song bouts by the addition of the only two male-specific phrases of the species' repertoire. These phrases differ from all others of the species and from vocalizations typical of the larger, nonhuman great apes, in that they contain rapid within-phrase modulation. Their modulation rates (6.82 and 7.34 Hz) are similar to that of lip-smacking in other nonhuman primates and speech in humans and, like human speech, are produced exclusively during exhalation. One phrase type (trills) contains multiple notes per exhalation, another characteristic similar to speech but not most primate vocalizations. Our data highlight the complexity and flexibility of gibbon song, and show that particular phrase features likely arose from sexual selection pressures and possess similarities to human speech rhythm.

So much for the city: Urban-rural song variation in a widespread Asiatic songbird.

Song plays a fundamental role in intraspecific communication in songbirds. The temporal and structural components of songs can vary in different habitats. These include urban habitats where anthropogenic sounds and alteration of habitat structure can significantly affect songbird vocal behavior. Urban-rural variations in song complexity, song length and syllable rate are not fully understood. In this study, using the oriental magpie-robin (Copsychus saularis) as a model, we investigated urban-rural variation in song complexity, song length, syllable rate, syllable length and inter-syllable interval. Comparing urban and rural songs from 7 countries across its natural Asiatic range (Bangladesh, India, Malaysia, Nepal, Singapore, Sri Lanka and Thailand), we found no significant differences in oriental magpie-robin song complexity. However, we found significant differences in temporal song variables between urban and rural sites. Longer songs and inter-syllable intervals in addition to slower syllable rates within urban sites contributed the most to this variance. This indicates that the urban environment may have driven production of longer and slower songs to maximize efficient transmission of important song information in urban habitats.

Birdsong characteristics are related to fragment size in a neotropical forest

The oscine passerines, an avian suborder that comprises almost half of all bird species worldwide, learn their song primarily through cultural transmission. As the world's forests become increasingly fragmented and the population sizes of many forest-dwelling species decline, there may be increasingly restricted opportunities for the transmission of cultural information. However, the effects of forest fragmentation on birdsong have not been well documented. In this paper, we examine the relationship between forest fragment size and song characteristics for two forest bird species, an oscine passerine (orange-billed sparrow, Arremon aurantiirostris) that learns its song culturally, and a suboscine passerine (scale-crested pygmy tyrant, Lophotriccus pileatus) that does not. Recordings were taken from individuals in 12 premontane wet forest fragments ranging in size from approximately 1.4 ha–360 ha in southern Costa Rica. As predicted under the ‘cultural erosion’ hypothesis, we found that acoustic characteristics associated with song complexity such as the number of syllables per song and song duration decreased with decreasing fragment size for the oscine but not for the suboscine species. This study supports the idea that learned cultural elements are sensitive to fragment size and that cultural diversity should be considered along with other forms of biodiversity in the conservation of social learning species.

The effect of isolation, fragmentation, and population bottlenecks on song structure of a Hawaiian honeycreeper.

Little is known about how important social behaviors such as song vary within and among populations for any of the endemic Hawaiian honeycreepers. Habitat loss and non‐native diseases (e.g., avian malaria) have resulted in isolation and fragmentation of Hawaiian honeycreepers within primarily high elevation forests. In this study, we examined how isolation of Hawai'i ‘amakihi (Chlorodrepanis virens) populations within a fragmented landscape influences acoustic variability in song. In the last decade, small, isolated populations of disease tolerant ‘amakihi have been found within low elevation forests, allowing us to record ‘amakihi songs across a large elevational gradient (10–1800 m) that parallels disease susceptibility on Hawai'i island. To understand underlying differences among populations, we examined the role of geographic distance, elevation, and habitat structure on acoustic characteristics of ‘amakihi songs. We found that the acoustic characteristics of ‘amakihi songs and song‐type repertoires varied most strongly across an elevational gradient. Differences in ‘amakihi song types were primarily driven by less complex songs (e.g., fewer frequency changes, shorter songs) of individuals recorded at low elevation sites compared to mid and high elevation populations. The reduced complexity of ‘amakihi songs at low elevation sites is most likely shaped by the effects of habitat fragmentation and a disease‐driven population bottleneck associated with avian malaria, and maintained through isolation, localized song learning and sharing, and cultural drift. These results highlight how a non‐native disease through its influence on population demographics may have also indirectly played a role in shaping the acoustic characteristics of a species.

Singing Patterns of Male Pied Bush Chats (Saxicola caprata) Across Years and Nesting Cycles

ABSTRACT.— We investigated singing patterns of Pied Bush Chats across years and nesting cycles. We recorded the seasonal singing activity of 25 males in their natural habitats in Haridwar, Himalayan foothills, India for three consecutive years. The vocal patterns, especially song repertoire size of males, remained largely constant, and this restricted annual variation suggests that the Pied Bush Chats are closed-end learners. Analysis of song bouts during different stages of the nesting cycle and across years indicates that the Pied Bush Chat is an immediate variety singer. The song output in terms of song complexity, song rate, song bout length, and percentage performance time was highest at the beginning of egg laying and during incubation compared to pre-nesting, nest building, and provisioning stages. Such singing peaks with respect to different stages of the nesting cycle indicated mate guarding by male Pied Bush Chats and announcement of fertility status of the guarded female.

Song structure and variability in the Black-headed Bunting (Emberiza melanocephala)

Fighting and flirting are the main evolutionary forces behind the development of bird song and both contribute to different song characteristics. By comparison of vocalisations throughout bird taxa, we can help to reconstruct the evolutionary history of the song. In this study, we provide the first detailed analysis of song structure and song type variability in the Black-headed Bunting (Emberiza melanocephala). We quantify the fine structural characteristics of the song and describe the song and syllable repertoire size. Further, we describe intraindividual song variability over time and interindividual song variability over space, and we explore whether this species uses syntactic rules to create songs. Our analyses reveal that the Black-headed Bunting has a short yet rather complex song and that the syllable pool is extensive. Its song is constructed of three parts that differ in both complexity and rhythm, suggesting the use of syntactic rules in constructing a song. The male song is typically built of 9–13 syllables, with 7–12 that are non-repetitive. Each male sings only one stereotyped song, which remains identical throughout the male’s lifespan, providing evidence for age-limited song learning. Songs are individually distinct, suggesting the importance of song in individual recognition of males. Two spatial levels of song variation in the Black-headed Bunting are shown. On a microgeographical level, relatively small song neighbourhoods are formed with a handful of birds singing the same song type. On a macrogeographical level, dialects can be distinguished by the end part of a song. The most striking feature of the male Black-headed Bunting song is the immense variability of song types. Typically, only a small number of males shared the same song type, and males with unique song types occurred frequently as well. The high song complexity and single-song repertoire found in the Black-headed Bunting could reflect a high level of polygyny and a low level of parental care, therefore pointing to strong intersexual selection on the male song.

Postnatal nutrition influences male attractiveness and promotes plasticity in male mating preferences.

Poor early-life nutrition could reduce adult reproductive success by negatively affecting traits linked to sexual attractiveness such as song complexity. If so, this might favor strategic mate choice, allowing males with less complex songs to tailor their mating tactics to maximize the reproductive benefits. However, this possibility has been ignored in theoretical and empirical studies. By manipulating the micronutrient content of the diet (e.g., low or high) during the postnatal period of male zebra finches, we show for the first time (1) that males reared on a poor (low) micronutrient diet had less complex songs as adults; (2) that these males, in contrast to the high micronutrient diet group, were more selective in their mating strategies, discriminating against those females most likely to reduce their clutch size when paired with males having less complex songs; and (3) that by following different mating strategies, males reared on the contrasting diets obtained similar reproductive benefits. These results suggest that early-life dietary conditions can induce multiple and long-lasting effects on male and female reproductive traits. Moreover, the results seem to reflect a previously unreported case of adaptive plasticity in mate choice in response to a nutritionally mediated reduction in sexual attractiveness.

Birdsong signals individual diversity at the major histocompatibility complex.

The major histocompatibility complex (MHC) plays a key role in vertebrate immunity, and pathogen-mediated selection often favours certain allelic combinations. Assessing potential mates' MHC profiles may provide receivers with genetic benefits (identifying MHC-compatible mates and producing optimally diverse offspring) and/or material benefits (identifying optimally diverse mates capable of high parental investment). Oscine songbirds learn songs during early life, such that song repertoire content can reflect population of origin while song complexity can reflect early life condition. Thus birdsong may advertise the singer's genetic dissimilarity to others in the population (and, presumably, compatibility with potential mates), or individual genetic diversity (and thus condition-dependent material benefits). We tested whether song repertoire content and/or complexity signal MHC class IIβ dissimilarity and/or diversity in male song sparrows (Melospiza melodia). Pairwise dissimilarity in repertoire content did not predict MHC dissimilarity between males, suggesting that locally rare songs do not signal rare MHC profiles. Thus, geographical variation in song may not facilitate MHC-mediated inbreeding or outbreeding. Larger repertoires were associated with intermediate MHC diversity, suggesting intermediate rather than maximal MHC diversity is optimal. This could reflect trade-offs between resisting infection and autoimmune disorders. Song complexity may advertise optimal MHC diversity, a trait affecting disease resistance and capacity for parental care.

Fighting talk: complex song elicits more aggressive responses in a vocally complex songbird

Song complexity in many songbirds is a trait subject to sexual selection. It is often associated with male territorial defence. Empirical studies testing differential male responses to rival song in vocally complex songbirds have, however, been scarce. We conducted playback experiments of the endemic New Zealand Tui Prosthemadera novaeseelandiae to test the aggressive response of territorial male Tui to rival songs with differing complexity levels. Overall, complex songs evoked significantly stronger responses from territorial males than did simple songs. Following playback of complex songs, focal males approached the playback more closely and rapidly, and responded with songs of higher complexity than they did to playback of simple songs. This suggests males could both distinguish between different levels of complexity within the Tui repertoire, and perceive a more complex song as a greater territorial threat. Our study is one of the first to demonstrate strong aggressive responses to increased levels of song complexity in a songbird species with highly complex vocalizations.