Large-scale analysis of frequency modulation in birdsong data bases

DS & MP are supported by an EPSRC Leadership Fellowship EP/G007144/1. Our thanks to Alan McElligott for helpful advice while preparing the manuscript; Sašo Muševič for discussion and for making his DDM software available; and Rémi Gribonval and team at INRIA Rennes for discussion and software development during a research visit

Automatic large-scale classification of bird sounds is strongly improved by unsupervised feature learning

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Mapping Acoustic and Semantic Dimensions of Auditory Perception

Auditory categorisation is a function of sensory perception which allows humans to generalise across many different sounds present in the environment and classify them into behaviourally relevant categories. These categories cover not only the variance of acoustic properties of the signal but also a wide variety of sound sources. However, it is unclear to what extent the acoustic structure of sound is associated with, and conveys, different facets of semantic category information. Whether people use such data and what drives their decisions when both acoustic and semantic information about the sound is available, also remains unknown. To answer these questions, we used the existing methods broadly practised in linguistics, acoustics and cognitive science, and bridged these domains by delineating their shared space. Firstly, we took a model-free exploratory approach to examine the underlying structure and inherent patterns in our dataset. To this end, we ran principal components, clustering and multidimensional scaling analyses. At the same time, we drew sound labels’ semantic space topography based on corpus-based word embeddings vectors. We then built an LDA model predicting class membership and compared the model-free approach and model predictions with the actual taxonomy. Finally, by conducting a series of web-based behavioural experiments, we investigated whether acoustic and semantic topographies relate to perceptual judgements. This analysis pipeline showed that natural sound categories could be successfully predicted based on the acoustic information alone and that perception of natural sound categories has some acoustic grounding. Results from our studies help to recognise the role of physical sound characteristics and their meaning in the process of sound perception and give an invaluable insight into the mechanisms governing the machine-based and human classifications

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

Assessing the Phylogenetic and Cultural Content of Learned Song

In the oscine songbirds, song is learned by a juvenile from a tutor of the same species, in a pattern that is analogous to human language, and likewise has the potential to change over time by cultural evolution. The similarities between human languages have been studied for centuries, but historically the relationships between the songs of birds of different species have been seen as too divergent to be useful. Using a computational analysis of song databases coupled with genetic phylogenies, I have shown that there is indeed a significant correlation between genetic distance and song similarity in the oscines. For a subset of Emberizid species, it was possible to reconstruct a genus-level phylogeny using the song syntax of these birds. For one member of this subset, I traced the cultural evolution of song properties, both over time and across distances. In addition, I examined the role of innate predispositions in song learning by hybridizing two species of Estrildid finches and examining the vocal output of hybrids in comparison with normally raised and cross-fostered birds. This work represents the first large-scale evolutionary analysis of learned song and the first clear demonstration of the relationship between genetic relatedness and song similarity

Public Engagement Technology for Bioacoustic Citizen Science

Inexpensive mobile devices offer new capabilities for non-specialist use in the field for the purpose of conservation. This thesis explores the potential for such devices to be used by citizen scientists interacting with bioacoustic data such as birdsong. This thesis describes design research and field evaluation, in collaboration with conservationists and educators, and technological artefacts implemented as mobile applications for interactive educational gaming and creative composition. This thesis considers, from a participant-centric collaborative design approach, conservationists' demand for interactive artefacts to motivate engagement in citizen science through gameful and playful interactions. Drawing on theories of motivation, frequently applied to the study of Human-Computer Interaction (HCI), and on approaches to designing for motivational engagement, this thesis introduces a novel pair of frameworks for the analysis of technological artefacts and for assessing participant engagement with bioacoustic citizen science from both game interaction design and citizen science project participation perspectives. This thesis reviews current theories of playful and gameful interaction developed for collaborative learning, data analysis, and ground-truth development, describes a process for design and analysis of motivational mobile games and toys, and explores the affordances of various game elements and mechanics for engaging participation in bioacoustic citizen science. This thesis proposes research into progressions for scaffolding engagement with citizen science projects where participants interact with data collection and analysis artefacts. The research process includes the development of multiple designs, analyses of which explore the efficacy of game interactions to motivate engagement through interaction progressions, given proposed analysis frameworks. This thesis presents analysed results of experiments examining the usability of, and data-quality from, several prototypes and software artefacts, in both laboratory conditions and the field. This thesis culminates with an assessment of the efficacy of proposed design analysis frameworks, an analysis of designed artefacts, and a discussion of how these designs increase intrinsic and extrinsic motivation for participant engagement and affect resultant bioacoustic citizen science data quantity and quality.Non

Molecular profiling of sex-specific development of song and the song control nucleus HVC of songbirds

Singing of songbird species is a behavior that integrates multiple sensory inputs and motor outputs, which primarily rely on interconnected neural circuits in the avian brain, the song control system. The nucleus HVC is of particular interest because of its integrative roles in the song control system. In the majority of Northern temperate songbird species, males sing predominately, and they often use their songs to attract female mates. In contrast, most Northern temperate female songbirds sing either rarely or only in certain contexts. The characteristics and functions of female songs are less clear. In the tropics, many species of females sing regularly and depending on species, their song complexity is less or comparable to that of males. However, the HVC volume is greater in males than females in all songbird species that have been examined. In the first experiment of this thesis (p. 43), I described song features of spontaneously and rarely singing female canaries (Serinus canaria), a Northern temperate songbird species. I observed higher blood testosterone concentrations and greater HVC volume of singing females than that of non-singing females. The results suggest female canary singing is testosterone-dependent. Subcutaneous testosterone implantation induces singing in female canaries. In the second experiment (p. 65), I implanted female canaries with testosterone for six time periods (T1h, T3h, T8h, T3d, T7d, and T14d) and studied changes of gene expression in the HVC. I observed approximately 2,600 genes regulated by testosterone after one hour and the regulation was dynamic throughout the experimental time window. I investigated putative biological functions of testosterone-regulated genes in the six time points by gene ontology (GO)-term enrichment analysis, and showed that the enrichment of angiogenesis began at T1h and the enrichment of neurogenesis began at T3h, with both processes continuing until T14d. Furthermore, genes associated with “GABA” and “spine” were enriched in T3d birds when the birds started singing, while the number of genes associated with “nervous system development” was highest in T14d birds, when the HVC volume was significantly greater than controls. Finally, using approaches integrating gene expression, HVC volume, circulating testosterone levels, and song characteristics, I identified a potential master regulator of testosterone-regulated changes. Male canary songs vary seasonally. Breeding season songs are longer, louder, and more complex than non-breeding season songs. Non-breeding males implanted with testosterone sing songs resembling that of breeding season songs. In the third experiment (p. 81), I studied gene expression in the HVC of seven canary groups, females and males of breeding season and of non-breeding season, non-breeding season females and males treated with testosterone, and spontaneously singing female canaries. Hierarchical clustering and principal component analysis (PCA) showed that circulating testosterone levels and sex were the predominant variables associated with variation in the HVC transcriptomes. Comparison between natural singing canaries with testosterone-induced singing canaries of the same sex revealed large differences in the HVC transcriptomes. Moreover, the intersection of natural and testosterone-induced singing females shared little resemblance with males in terms of genes. GO-term enrichment analysis suggested functional overlap between sex-specific gene networks. However, although strong transcriptional changes in HVC correlate with the transition from non-singing to singing in both sexes, the type of transcriptional changes are sex-specific. In the fourth experiment (p. 89), I studied sex differences in HVC gene expression between three songbird species: the canary, the blue-capped cordon bleus (Uraeginthus cyanocephalus), and the forest weavers (Ploceus bicolor). Cordon bleu females sing regularly with female-specific songs, whereas forest weaver females sing songs identical to males. I found substantial sex differences in HVC gene expression in all three species, and sex-biased genes differed between species. Surprisingly, the majority of sex-biased genes were on autosomes instead the sex chromosome Z. These results provide further evidence for sex differences in brain structure at the molecular and cellular levels in sexually reproductive animals

Molecular profiling of sex-specific development of song and the song control nucleus HVC of songbirds

Singing of songbird species is a behavior that integrates multiple sensory inputs and motor outputs, which primarily rely on interconnected neural circuits in the avian brain, the song control system. The nucleus HVC is of particular interest because of its integrative roles in the song control system. In the majority of Northern temperate songbird species, males sing predominately, and they often use their songs to attract female mates. In contrast, most Northern temperate female songbirds sing either rarely or only in certain contexts. The characteristics and functions of female songs are less clear. In the tropics, many species of females sing regularly and depending on species, their song complexity is less or comparable to that of males. However, the HVC volume is greater in males than females in all songbird species that have been examined. In the first experiment of this thesis (p. 43), I described song features of spontaneously and rarely singing female canaries (Serinus canaria), a Northern temperate songbird species. I observed higher blood testosterone concentrations and greater HVC volume of singing females than that of non-singing females. The results suggest female canary singing is testosterone-dependent. Subcutaneous testosterone implantation induces singing in female canaries. In the second experiment (p. 65), I implanted female canaries with testosterone for six time periods (T1h, T3h, T8h, T3d, T7d, and T14d) and studied changes of gene expression in the HVC. I observed approximately 2,600 genes regulated by testosterone after one hour and the regulation was dynamic throughout the experimental time window. I investigated putative biological functions of testosterone-regulated genes in the six time points by gene ontology (GO)-term enrichment analysis, and showed that the enrichment of angiogenesis began at T1h and the enrichment of neurogenesis began at T3h, with both processes continuing until T14d. Furthermore, genes associated with “GABA” and “spine” were enriched in T3d birds when the birds started singing, while the number of genes associated with “nervous system development” was highest in T14d birds, when the HVC volume was significantly greater than controls. Finally, using approaches integrating gene expression, HVC volume, circulating testosterone levels, and song characteristics, I identified a potential master regulator of testosterone-regulated changes. Male canary songs vary seasonally. Breeding season songs are longer, louder, and more complex than non-breeding season songs. Non-breeding males implanted with testosterone sing songs resembling that of breeding season songs. In the third experiment (p. 81), I studied gene expression in the HVC of seven canary groups, females and males of breeding season and of non-breeding season, non-breeding season females and males treated with testosterone, and spontaneously singing female canaries. Hierarchical clustering and principal component analysis (PCA) showed that circulating testosterone levels and sex were the predominant variables associated with variation in the HVC transcriptomes. Comparison between natural singing canaries with testosterone-induced singing canaries of the same sex revealed large differences in the HVC transcriptomes. Moreover, the intersection of natural and testosterone-induced singing females shared little resemblance with males in terms of genes. GO-term enrichment analysis suggested functional overlap between sex-specific gene networks. However, although strong transcriptional changes in HVC correlate with the transition from non-singing to singing in both sexes, the type of transcriptional changes are sex-specific. In the fourth experiment (p. 89), I studied sex differences in HVC gene expression between three songbird species: the canary, the blue-capped cordon bleus (Uraeginthus cyanocephalus), and the forest weavers (Ploceus bicolor). Cordon bleu females sing regularly with female-specific songs, whereas forest weaver females sing songs identical to males. I found substantial sex differences in HVC gene expression in all three species, and sex-biased genes differed between species. Surprisingly, the majority of sex-biased genes were on autosomes instead the sex chromosome Z. These results provide further evidence for sex differences in brain structure at the molecular and cellular levels in sexually reproductive animals