Quantitative Tools for Examining the Vocalizations of Juvenile Songbirds

The singing of juvenile songbirds is highly variable and not well stereotyped, a feature that makes it difficult to analyze with existing computational techniques. We present here a method suitable for analyzing such vocalizations, windowed spectral pattern recognition (WSPR). Rather than performing pairwise sample comparisons, WSPR measures the typicality of a sample against a large sample set. We also illustrate how WSPR can be used to perform a variety of tasks, such as sample classification, song ontogeny measurement, and song variability measurement. Finally, we present a novel measure, based on WSPR, for quantifying the apparent complexity of a bird's singing

Variability in Singing and in Song in the Zebra Finch

Variability is a defining feature of the oscine song learning process, reflected in song and in the neural pathways involved in song learning. For the zebra finch, juveniles learning to sing typically exhibit a high degree of vocal variability, and this variability appears to be driven by a key brain nucleus. It has been suggested that this variability is a necessary part of a trial-­â€and-­â€error learning process in which the bird must search for possible improvements to its song. Our work examines the role this variability plays in learning in two ways: through behavioral experiments with juvenile zebra finches, and through a computational model of parts of the oscine brain. Previous studies have shown that some finches exhibit less variability during the learning process than others by producing repetitive vocalizations. A constantly changing song model was played to juvenile zebra finches to determine whether auditory stimuli can affect this behavior. This stimulus was shown to cause an overall increase in repetitiveness; furthermore, there was a correlation between repetitiveness at an early stage in the learning process and the length of time a bird is repetitive overall, and birds that were repetitive tended to repeat the same thing over an extended period of time. The role of a key brain nucleus involved in song learning was examined through computational modeling. Previous studies have shown that this nucleus produces variability in song, but can also bias the song of a bird in such a way as to reduce errors while singing. Activity within this nucleus during singing is predominantly uncorrelated with the timing of the song, however a portion of this activity is correlated in such a manner. The modeling experiments consider the possibility that this persistent signal is part of a trial-­â€and-­â€error search and contrast this with the possibility that the persistent signal is the product of some mechanism to directly improve song. Simulation results show that a mixture of timing-­â€dependent and timing-­â€independent activity in this nucleus produces optimal learning results for the case where the persistent signal is a key component of a trial-­â€and-­â€error search, but not in the case where this signal will directly improve song. Although a mixture of timing-­â€locked and timing-­â€independent activity produces optimal results, the ratio found to be optimal within the model differs from what has been observed in vivo. Finally, novel methods for the analysis of birdsong, motivated by the high variability of juvenile song, are presented. These methods are designed to work with sets of song samples rather than through pairwise comparison. The utility of these methods is demonstrated, as well as results illustrating how such methods can be used as the basis for aggregate measures of song such as repertoire complexity

Variable Food Begging Calls Are Harbingers of Vocal Learning

Vocal learning has evolved in only a few groups of mammals and birds. The developmental and evolutionary origins of vocal learning remain unclear. The imitation of a memorized sound is a clear example of vocal learning, but is that when vocal learning starts? Here we use an ontogenetic approach to examine how vocal learning emerges in a songbird, the chipping sparrow. The first vocalizations of songbirds, food begging calls, were thought to be innate, and vocal learning emerges later during subsong, a behavior reminiscent of infant babbling. Here we report that the food begging calls of male sparrows show several characteristics associated with learned song: male begging calls are highly variable between individuals and are altered by deafening; the production of food begging calls induces c-fos expression in a forebrain motor nucleus, RA, that is involved with the production of learned song. Electrolytic lesions of RA significantly reduce the variability of male calls. The male begging calls are subsequently incorporated into subsong, which in turn transitions into recognizable attempts at vocal imitation. Females do not sing and their begging calls are not affected by deafening or RA lesion. Our results suggest that, in chipping sparrows, intact hearing can influence the quality of male begging calls, auditory-sensitive vocal variability during food begging calls is the first step in a modification of vocal output that eventually culminates with vocal imitation

The nocturnal flight calls of migratory songbirds: interspecific variation in the “zeep” complex and intraspecific variation across North America

The nocturnal flight calls of birds are short vocalizations, produced primarily during migration. Although these calls offer a unique opportunity for studying avian migration, there has been little research into many aspects of these calls, such as the species-specificity of the calls of closely related taxa, or variation in calls associated with age, sex, or geography. The objective of my thesis research was to investigate acoustic variation within the flight calls of songbirds to expand our understanding of these calls and their application in migration monitoring. I recorded the flight calls of birds held for banding as well as birds actively flying during their nocturnal movements. In my first data chapter, I investigated whether the nocturnal flight calls of nine warbler species (i.e. the “zeep” species-group) exhibited acoustic differences. Analysis of the acoustic properties of flight calls of these species revealed significant differences in call structure between species, including five species that were notably different from the others in one or more acoustic properties. My results revealed that flight calls could be assigned to the correct species more often (73%) than expected by chance (36%), although the classification was not perfect. Therefore, acoustic variation in the flight calls of the “zeep” complex can be used to identify more species than previously thought. In my second data chapter, I explored intraspecific variation in flight calls. I found no evidence of sex-based or age-based variation in three species, and no evidence of geographic variation in two species. Although I found geographic variation in the calls of Dark-eyed Juncos, there was no consistent pattern on an east-west axis. Together, these results provided very little evidence for variation in flight calls with sex or age and limited evidence for geographic variation. Consequently, flight calls may be used to identify species (or species-groups) but not to identify sex, age, or geographic origin. My research serves to enhance the capabilities of nocturnal flight call detections for monitoring migratory birds while improving our understanding of drivers of variation in these calls

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

THE ROLE OF MELATONIN IN BIOLOGICAL RHYTHMS OF SONGBIRDS

In vertebrates, melatonin is a hormone that is produced and secreted at night and inhibited by light. This unique “darkness-only” expression profile makes it an intellectually appealing candidate for a means of transmitting temporal information to an individual, both time of day and time of year. In passerine birds, “time of day” information is certainly transmitted via melatonin secretion. The primary producer of systemic melatonin in this family of birds is the pineal gland, and surgical removal of it causes a bird to become arrhythmic in constant conditions. I find that as pinealectomized house sparrows (Passer domesticus) become behaviorally arrhythmic in extended constant darkness the molecular clock in their peripheral tissues largely continues to cycle absent its hypothesized synchronizing cues from the pineal gland. This suggests that the peripheral tissues are either autonomous or that there is a possible secondary circadian oscillator that synchronizes these tissues, such as the avian suprachiasmatic nucleus. In passerine birds, “time of year” information is not transmitted via melatonin secretion to the primary gonads, unlike the case in seasonally breeding mammals. The duration of melatonin, longer in the winter and shorter in the spring as the photoperiod changes with the seasons, does affect secondary sexual characteristics, such as the vocal behavior of birds and the size of the associated nuclei in the brain. I find that long durations of melatonin are sufficient in preventing the photoperiodic expansion of vocal state in male house sparrows. This vocal state change in males consists of the development of a dawn and dusk chorus, as well as a switch from a vocal subtype associated with the wintertime birds flocking together to one of mate attraction and territory defense. This dynamic was independent of the size of the gonads, which were consistent those of photostimulated males. I also investigate this vocal state change in outdoor captive sparrows. This vocal state change is also present in female house sparrows, although unlike in male birds, the presence of absence of the pineal gland does not affect the timing of their vocalizations. Further, I investigate the ability for rhythmic presentations of vocalizations to influence the circadian clock, in zebra finches, Taeniopygia guttata. Aural cues have been shown to act as a weak external cue for entraining a passerine bird’s circadian clock. I presented various permutations of zebra finch vocalization: a single song played repeatedly, the same song played reversed, random tones, and live monitoring of a breeding colony entrained to a light-dark cycle. The live monitoring was the strongest aural cue, and more generally it appears that novelty and context enhance the effect of audio cues on the circadian clock. These experiments in sum suggest a role of melatonin in gating the seasonal expression of vocalization behavior in house sparrows. In male birds, a component of the seasonal dynamic is the development of a multimodal rhythm to when during the day the birds vocalize as the days lengthen consistent with spring, suggesting that the circadian clock may be involved with this diel variability. Additionally, this vocal behavior can also feedback onto the circadian clock. The pineal gland and its primary hormone melatonin function, in part, to regulate complex behavioral rhythms in passerine birds

Dialects in animals: Evidence, development and potential functions

International audienceDialects are one of the parallels that have long been established between human language and animal communication. We discuss the potential functional parallels between human and animal dialects, arguing that in both cases different mechanisms and functions may be at stake where large geographical versus very localized (e.g. social) variations are concerned. Birdsong studies in particular, but also recent studies of mammal vocalizations, show that the use of the term “dialect” to refer to within-species vocal variations in animal species is more than a metaphor and that animal dialects offer a possibility to explore the causes and functions of linguistic variation and change, one of the challenges in exploring the origin of diversity of language families. We present here an original view, as our approach was not "primate-centered" and take into consideration “homoplasy” (analogy) as a potential mechanism to explain that different taxa have evolved the same functional response to social constraints

Vocal Learning in the Costa's Hummingbird

Here I examine vocal learning in the Costa’s hummingbird. I used the standard isolation experiment technique utilized for decades to study vocal learning in songbirds. Young male Costa’s hummingbirds were raised in isolation, with playback of adult song, and with playback in the presence of an adult model. All bird vocalizations were recorded to examine song ontogeny. I found that the necessary conditions required for vocal learning of a tutor song to take place in a lab setting included the presence of an adult model during tutoring and the tutor song must be Costa’s like. I developed a timeline of song ontogeny events including information about the onset of singing, and the stages of song development. Another experiment examined the timing of the sensitive phase by tutoring Costa’s for 20 hours in one of three different 30-day tutoring periods: Early (35-65 days post hatch (dph)), Mid (75-105 dph), and Late (115-145 dph). Results indicated that Costa’s can learn some vocal information across all three tutoring periods but that the amount of tutoring during one tutoring period was insufficient for production of normal Costa’s song. Finally, I examined open-ended vocal learning by exposing previously isolated birds to other Costa’s hummingbirds and found that songs change after exposure, even after two years of isolation

New horizons for female birdsong : evolution, culture and analysis tools : a thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Ecology at Massey University, Auckland, New Zealand

Published papers appear in Appendix 7.1. and 7.2 respectively under a CC BY 4.0 and CC BY licence: Webb, W. H., Brunton, D. H., Aguirre, J. D., Thomas, D. B., Valcu, M., & Dale, J. (2016). Female song occurs in songbirds with more elaborate female coloration and reduced sexual dichromatism. Frontiers in Ecology and Evolution, 4(22). https://doi.org/10.3389/fevo.2016.00022 Yukio Fukuzawa, Wesley Webb, Matthew Pawley, Michelle Roper, Stephen Marsland, Dianne Brunton, & Andrew Gilman. (2020). Koe: Web-based software to classify acoustic units and analyse sequence structure in animal vocalisations. Methods in Ecology and Evolution, 11(3). https://doi.org/10.1111/2041-210X.13336As a result of male-centric, northern-hemisphere-biased sexual selection theory, elaborate female traits in songbirds have been largely overlooked as unusual or non-functional by-products of male evolution. However, recent research has revealed that female song is present in most surveyed songbirds and was in fact the ancestral condition to the clade. Additionally, a high proportion of songbird species have colourful females, and both song and showy colours have demonstrated female-specific functions in a growing number of species. We have much to learn about the evolution and functions of elaborate female traits in general, and female song in particular. This thesis extends the horizons of female birdsong research in three ways: (1) by revealing the broad-scale evolutionary relationship of female song and plumage elaboration across the songbirds, (2) by developing new accessible tools for the measurement and analysis of song complexity, and (3) by showing—through a detailed field study on a large natural metapopulation—how vocal culture operates differentially in males and females. First, to understand the drivers of elaborate female traits, I tested the evolutionary relationship between female song presence and plumage colouration across the songbirds. I found strong support for a positive evolutionary correlation between traits, with female song more prevalent amongst species with elaborated female plumage. These results suggest that contrary to the idea of trade-off between showy traits, female plumage colouration and female song likely evolved together under similar selection pressures and that their respective functions are reinforcing. Second, I introduce new bioacoustics software, Koe, designed to meet the need for detailed classification and analysis of song complexity. The program enables visualisation, segmentation, rapid classification and analysis of song structure. I demonstrate Koe with a case study of New Zealand bellbird Anthornis melanura song, showcasing the capabilities for large-scale bioacoustics research and its application to female song. Third, I conducted one of the first detailed field-based analyses of female song culture, studying an archipelago metapopulation of New Zealand bellbirds. Comparing between male and female sectors of each population, I found equal syllable diversity, largely separate repertoires, and contrasting patterns of sharing between sites—revealing female dialects and pronounced sex differences in cultural evolution. By combining broad-scale evolutionary approaches, novel song analysis tools, and a detailed field study, this thesis demonstrates that female song can be as much an elaborate signal as male song. I describe how future work can build on these findings to expand understanding of elaborate female traits