Responses to song playback differ in sleeping versus anesthetized songbirds

Vocal learning in songbirds is mediated by a highly localized system of interconnected forebrain regions, including recurrent loops that traverse the cortex, basal ganglia, and thalamus. This brain-behavior system provides a powerful model for elucidating mechanisms of vocal learning, with implications for learning speech in human infants, as well as for advancing our understanding of skill learning in general. A long history of experiments in this area has tested neural responses to playback of different song stimuli in anesthetized birds at different stages of vocal development. These studies have demonstrated selectivity for different song types that provide neural signatures of learning. In contrast to the ease of obtaining responses to song playback in anesthetized birds, song-evoked responses in awake birds are greatly reduced or absent, indicating that behavioral state is an important determinant of neural responsivity. Song-evoked responses can be elicited in sleeping as well as anesthetized zebra finches, and the selectivity of responses to song playback in adult birds tends to be highly similar between anesthetized and sleeping states, encouraging the idea that anesthesia and sleep are highly similar. In contrast to that idea, we report evidence that cortical responses to song playback in juvenile zebra finches (Taeniopygia guttata) differ greatly between sleep and urethane anesthesia. This finding indicates that behavioral states differ in sleep versus anesthesia and raises questions about relationships between developmental changes in sleep activity, selectivity for different song types, and the neural substrate for vocal learning.

Song type variations of Louisiana Waterthrush (Parkesia motacilla) and their geographic distributions

Louisiana Waterthrush (Parkesia motacilla) is a familiar singer in the Western Hemisphere family Parulidae, yet apparent geographic variations in its song and potentially related causal mechanisms have not received detailed examination in previously published studies. Here, we analyzed song pattern variations of 651 Louisiana Waterthrush singers in audio spectrogram recordings obtained from our field work and publicly accessible bioacoustics archives. Visual and auditory assessment of the introductory note sequence of each song identified three distinct song types (A, B, and C) and most of the songs were assigned to one of these types. Linear Discriminant Analysis and Random Forest methods were used to verify the assignments and showed strong agreement for Type A with slightly less agreement on Types B and C. User error rates (proportion of the Linear Discriminant Analysis classifications that were incorrect) were low for Types A and B, and somewhat higher for Type C, while producer error rates (proportion of the song type for which the Linear Discriminant Analysis was incorrect) were somewhat higher for Types A and C than the minimal levels achieved for Type B. Our findings confirmed that most between-individual variation was in the number of notes and note sequence duration while most within-individual variation resulted from the percent of downstrokes. The location of each singer was plotted on a map of the breeding range and results suggested the song types have large-scale discrete geographic distributions that co-occur in some regions but not range-wide. Evaluation of the distributions provided tentative support for a hypothesis that two of the song types may independently exhibit congruence with the geographic extent of Pleistocene glacial boundaries and the third song type may be distinguished by a lack of congruence, but further investigation is needed to elucidate whether the song variations represent subpopulations with three separate evolutionary histories.

Fin whale acoustic populations present in New Zealand waters: Description of song types, occurrence and seasonality using passive acoustic monitoring

Southern fin whales (Balaenoptera physalus) are known to migrate from the Antarctic to mid-latitudes during winter for breeding, but the occurrence and distribution of this species is not well known in the waters around New Zealand. The ‘doublet’ calls are one of the main calls emitted specifically by fin whales and repeated in a regular pattern, which make the acoustic detection of these calls relevant to detect the presence of fin whales. Using a signal processing algorithm to detect ‘doublet’ calls emitted by fin whales, we studied the occurrence, characteristics and seasonality of these ‘doublet’ calls in two regions around New Zealand; Cook Strait in 2016/2017 and offshore Gisborne in 2014/2015. The call detection procedure consisted of binarization of the spectrogram and a cross-correlation between the binarized spectrogram and a template of binarized ‘doublet’ calls spectrogram. A binarization threshold for the data spectrograms and a cross correlation threshold were then determined through multiple trials on a training dataset and a Receiver Operating Characteristics (ROC) curve. Fin whale ‘doublet’ calls occurred on the east side of New Zealand’s Cook Strait during austral winter, specifically in June 2017 and offshore Gisborne in June-August 2014. No ‘doublet’ calls were detected on the west side of Cook Strait. The ‘doublet’ calls’ Inter-Note Interval (INI) was similar in both datasets. However, there was a difference in alternation of the mean frequency for both HF components of ‘doublet’ calls in Cook Strait and Gisborne. As the song types were compared with those previously described in the literature, our findings suggest that some fin whales wintering in New Zealand waters may be part of a broader ‘acoustic population’ whose range extends west to southern Australia and south to Antarctica.

Age-Related Testosterone Changes and Corresponding Song Patterns in Red-whiskered Bulbul (Pycnonotus jocosus Linnaeus, 1758)

We monitored total testosterone profiles and song patterns of 12 males and 2 females Red-whiskered Bulbuls (Pycnonotus jocosus), aged 5-10 months. Each bird was maintained in a cage sized of 38 × 38 × 50 cm and raised in a 22 °C-controlled room-sized of 6 × 10 × 3.5 m. The song prototype was played during 0700-11.00 h, with an amplifier-connected loudspeaker placed at the center and the song was recorded during both 1100-1200 and 1300-1500 h, and then their sonograms were analyzed with Avisoft SAS Lab Pro, version 4.3. Feces were collected monthly and immediately following recording their songs to determine male and female total testosterone levels by radioimmunoassay. The results demonstrated that an average of a frequency that the male and the female birds produced was 4.27 ± 0.13 kHz with a frequency range of 1.50 - 5.18 kHz. The males aged 8-10 months old produced songs with an average of 25.83 syllables/10 s, similar to those found in the song prototype while the females produced those with an average of 18.33 syllables/10 s. The males produced songs consisting of more syllables and fewer intervals than those of the females. The coefficient of correlations between the mean total testosterone levels with the syllables/10 s and intervals/10 s were +0.68 and -0.69, respectively. Additionally, the male Red-whiskered Bulbuls created the complicated and various song types that corresponded well with the marked increases in the total testosterone levels at the age of 8 to 10 months old.

Does the choosiness of female crickets change as they age?

For crickets, which approach singing males by phonotaxis, the female choosiness hypothesis postulates that young females should be more selective of male calling song patterns than older individuals. However, there is no information about the behavioural preferences of females over their complete adulthood. We analysed phonotaxis in female Gryllus bimaculatus throughout their entire adult lifetime and measured the impact of sound amplitude, carrier frequency, and the temporal pattern of test songs on their auditory response. Females of all ages demonstrated their best responses to male calling songs with a pulse period of 34-42 ms, a carrier frequency of 4.5 kHz and a sound pressure level of 75dB SPL. The response profile to somewhat less optimal song types did vary with age, but not in a manner consistent with a simple loosening of selectiveness in older females. Age however had an effect on the overall strength of phonotaxis, as very old females showed an overall diminishing response to all song types. Our data suggest that although there are minor changes in the relative preferences of crickets to individual song elements as they age, the breadth of song patterns that they will perform phonotaxis to remains similar across age groups.

SongExplorer: A deep learning workflow for discovery and segmentation of animal acoustic communication signals

Many animals produce distinct sounds or substrate-borne vibrations, but these signals have proved challenging to segment with automated algorithms. We have developed SongExplorer, a web-browser based interface wrapped around a deep-learning algorithm that supports an interactive workflow for (1) discovery of animal sounds, (2) manual annotation, (3) supervised training of a deep convolutional neural network, and (4) automated segmentation of recordings. Raw data can be explored by simultaneously examining song events, both individually and in the context of the entire recording, watching synced video, and listening to song. We provide a simple way to visualize many song events from large datasets within an interactive low-dimensional visualization, which facilitates detection and correction of incorrectly labelled song events. The machine learning model we implemented displays higher accuracy than existing heuristic algorithms and similar accuracy as two expert human annotators. We show that SongExplorer allows rapid detection of all song types from new species and of novel song types in previously well-studied species.

Decreased synthesis and variable gene transcripts of oxytocin in a domesticated avian species

The Bengalese finch was domesticated more than 250 years ago from the wild white-rumped munia. Similar to other domesticated species, Bengalese finches show a reduced fear response and have lower corticosterone levels, compared to white-rumped munias. Bengalese finches and munias also have different song types. Since oxytocin (OT) has been found to be involved in stress coping and auditory processing, we tested whether the OT sequence and brain expression pattern and content differ in wild munias and domesticated Bengalese finches. We identified intra-strain variability in the untranslated regions of the OT sequence in Bengalese finches in comparison to the munia OT. Several of these changes fall in specific transcription factor binding sites, which show either a conserved or a relaxed evolutionary trend in the avian lineage, and in vertebrates in general. Although in situ hybridization in several hypothalamic nuclei did not reveal significant differences in the number of cells expressing OT between the two strains, real-time quantitative PCR showed significantly lower OT mRNA expression in the diencephalon of the Bengalese finches relative to munias. Our study thus points to a decreased OT synthesis in the domestic strain compared with the wild strain in birds. This is an opposite pattern from that found in some domesticated mammals, suggesting that different processes of OT function might have occurred in mammals and birds under domestication.

Female and male song exhibit both parallel and divergent patterns of cultural evolution: A long-term study of song structure and diversity in tropical wrens

Animal culture changes over time through processes that include drift, immigration, selection, and innovation. Cultural change has been particularly well-studied for animal vocalizations, especially for the vocalizations of male animals in the temperate zone. Here we examine the cultural change in the vocalizations of tropical Rufous-and-white Wrens (Thryophilus rufalbus), quantifying temporal variation in song structure, song type diversity, and population-level distribution of song types in both males and females. We use data from 10 microsatellite loci to quantify patterns of immigration and neutral genetic differentiation over time, to investigate whether cultural diversity changes with rates of immigration. Based on 11 yr of data, we show that the spectro-temporal features of several widely-used persistent song types maintain a relatively high level of consistency for both males and females, whereas the distribution and frequency of particular song types change over time for both sexes. Males and females exhibit comparable levels of cultural diversity (i.e. the diversity of song types across the population), although females exhibit greater rates of cultural change over time. We found that female changes in cultural diversity increased when immigration is high, whereas male cultural diversity did not change with immigration. Our study is the first long-term study to explore cultural evolution for both male and female birds and suggests that cultural patterns exhibit notable differences between the sexes.