A potential neural substrate for processing functional classes of complex acoustic signals

Categorization is essential to all cognitive processes, but identifying the neural substrates underlying categorization processes is a real challenge. Among animals that have been shown to be able of categorization, songbirds are particularly interesting because they provide researchers with clear examples of categories of acoustic signals allowing different levels of recognition, and they possess a system of specialized brain structures found only in birds that learn to sing: the song system. Moreover, an avian brain nucleus that is analogous to the mammalian secondary auditory cortex (the caudo-medial nidopallium, or NCM) has recently emerged as a plausible site for sensory representation of birdsong, and appears as a well positioned brain region for categorization of songs. Hence, we tested responses in this non-primary, associative area to clear and distinct classes of songs with different functions and social values, and for a possible correspondence between these responses and the functional aspects of songs, in a highly social songbird species: the European starling. Our results clearly show differential neuronal responses to the ethologically defined classes of songs, both in the number of neurons responding, and in the response magnitude of these neurons. Most importantly, these differential responses corresponded to the functional classes of songs, with increasing activation from non-specific to species-specific and from species-specific to individual-specific sounds. These data therefore suggest a potential neural substrate for sorting natural communication signals into categories, and for individual vocal recognition of same-species members. Given the many parallels that exist between birdsong and speech, these results may contribute to a better understanding of the neural bases of speech.     

Novel motor gestures for phonation during inspiration enhance the acoustic complexity of birdsong.

Sound generation based on a pulmonary mechanism typically occurs during the expiratory phase of respiration. Phonation during inspiration has been postulated for the calls of some amphibians and for exceptional sounds in some human languages. No direct evidence exists for phonation during inspiration in birds, but such a mechanism has been proposed to explain very long uninterrupted songs. Here, we report the first physiological evidence for inspiratory sound production in the song of the zebra finch (Taeniopygia guttata). Motor gestures of the vocal and respiratory muscles leading to the production of inspiratory phonation differ from those of silent inspirations during song as well as from those leading to phonation during expiration. Inspiratory syllables have a high fundamental frequency, which makes them acoustically distinct from all other zebra finch song syllables. Furthermore, young zebra finches copy these inspiratory syllables from their tutor song, producing them during inspiration. This suggests that physical limitations confine the production of these sounds to the inspiratory phase in zebra finches. These findings directly demonstrate how novel respiratory-vocal coordination can enhance the acoustic structure of birdsong, and thus provide insight into the evolution of song complexity.     

THE COMMUNICATIVE SIGNIFICANCE OF TONALITY IN BIRDSONG: RESPONSES TO SONGS PRODUCED IN HELIUM

ABSTRACT

“Pure tones” are a distinctive acoustic feature of many birdsongs. Recent research on songbird vocal physiology suggests that such tonal sounds result from a coordinated interaction between the syrinx and a vocal filter, as demonstrated by the emergence of harmonic overtones when a bird sings in helium. To investigate the communicative significance of vocal tract filtration in the production of birdsong, we used field playback experiments to compare the responses of male swamp sparrows Melospiza georgiana to normal songs and those same songs recorded in helium. We also measured responses to pure tone songs that had been shifted upward in frequency to match the average spectra of those songs with added harmonics. Male sparrows were significantly more responsive to the playback of normal songs than to either helium songs with added harmonics or frequency- shifted pure tone songs. Songs with harmonics retained a high degree of salience, however. We conclude that explanations for the occurrence of tonal sounds in birdsongs must consider perceptual attributes of songs as communicative signals, as well as problems of song production and transmission.     

The impact of environmental factors in birdsong acquisition using automated recorders

The use of automatic acoustic recorders is becoming a principal method to survey birds in their natural habitats, as it is relatively noninvasive while still being informative. As with any other sound, birdsong degrades in amplitude, frequency, and temporal structure as it propagates to the recorder through the environment. Knowing how different birdsongs attenuate under different conditions is useful to, for example, develop protocols for deploying acoustic recorders and improve automated detection methods, an essential part of the research field that is becoming known as ecoacoustics. This article presents playback and recapture (record) experiments carried out under different environmental conditions using twenty bird calls from eleven New Zealand bird species in a native forest and an open area, answering five research questions: (1) How does birdsong attenuation differ between forest and open space? (2) What is the relationship between transmission height and birdsong attenuation? (3) How does frequency of birdsong impact the degradation of sound with distance? (4) Is birdsong attenuation different during the night compared to the day? and (5) what is the impact of wind on attenuation? Bird calls are complex sounds; therefore, we have chosen to use them rather than simple tones to ensure that this complexity is not missed in the analysis. The results demonstrate that birdsong transmission was significantly better in the forest than in the open site. During the night, the attenuation was at a minimum in both experimental sites. Transmission height affected the propagation of the songs of many species, particularly the flightless ones. The effect of wind was severe in the open site and attenuated lower frequencies. The reverberations due to reflective surfaces masked higher frequencies (8 kHz) in the forest even at moderate distances. The findings presented here can be applied to develop protocols for passive acoustic monitoring. Even though the attenuation can be generalized to frequency bands, the structure of the birdsong is also important. Selecting a reasonable sampling frequency avoids unnecessary data accumulation because higher frequencies attenuate more in the forest. Even at moderate distances, recorders capture significantly attenuated birdsong, and hence, automated analysis methods for field recordings need to be able to detect and recognize faint birdsong.     

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.     

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.     

Is the Tonal Quality of Birdsong Learned? Evidence from Song Sparrows

Song sparrow (Melospiza melodia) songs are composed largely of pure-tonal sounds. This paper investigates the role that learning plays in the development of the tonal structure of song sparrow songs, as well as the role that tonal quality plays in determining the suitability of songs as models for learning. 20 birds were trained with both normal pure-tonal songs and modified songs that included harmonic overtones. The harmonic-modified songs were obtained from birds singing in a helium atmosphere, the result of which is to perturb vocal tract resonances and thus alter a song's tonal quality. Subjects learned equally well from normal and harmonic models. Birds that learned material from harmonic models reproduced some of this material with harmonic overtones, but the majority of notes learned from harmonic models were subsequently reproduced as pure-tonal copies. Thus, the tonal structure of songs does not influence young song sparrows in their selection of song models, but there is a strong tendency to reproduce songs in a pure-tonal fashion, even if learned from harmonic models.     

Long-time storage of song types in birds: evidence from interactive playbacks

In studies of birdsong learning, imitation-based assays of stimulus memorization do not take into account that tutored song types may have been stored, but were not retrieved from memory. Such a 'silent' reservoir of song material could be used later in the bird's life, e.g. during vocal interactions. We examined this possibility in hand-reared nightingales during their second year. The males had been exposed to songs, both as fledglings and later, during their first full song period in an interactive playback design. Our design allowed us to compare the performance of imitations from the following categories: (i) songs only experienced during the early tutoring; (ii) songs experienced both during early tutoring and interactive playbacks; and (iii) novel songs experienced only during the simulated interactions. In their second year, birds imitated song types from each category, including those from categories (i) and (ii) which they had failed to imitate before. In addition, the performance of these song types was different (category (ii) > category (i)) and more pronounced than for category (iii) songs. Our results demonstrate 'silent' song storage in nightingales and point to a graded influence of the time and the social context of experience on subsequent vocal imitation.     

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.     

Preference for consonant music over dissonant music by an infant chimpanzee

It has been shown that humans prefer consonant sounds from the early stages of development. From a comparative psychological perspective, although previous studies have shown that birds and monkeys can discriminate between consonant and dissonant sounds, it remains unclear whether nonhumans have a spontaneous preference for consonant music over dissonant music as humans do. We report here that a five-month-old human-raised chimpanzee (Pan troglodytes) preferred consonant music. The infant chimpanzee consistently preferred to produce, with the aid of our computerized setup, consonant versions of music for a longer duration than dissonant versions. This result suggests that the preference for consonance is not unique to humans. Further, it supports the hypothesis that one major basis of musical appreciation has some evolutionary origins.     

A species-specific acoustic cue for selective song learning in the white-crowned sparrow

Song learning in birds is paradoxical. Without tutoring, songbirds do not develop normal songs. Yet despite this inability, birds possess extensive foreknowledge, in a mechanistic sense, about the normal song of their species. When given a choice of tape recordings, young, n?ive songbirds select sounds of their own species for imitation. We tape-tutored white-crowned sparrows, Zonotrichia leucophrys oriantha, with a set of manipulated songs to investigate whether the introductory whistle universally present in white-crowned sparrow song guides selective song learning in this species. Our results confirm that this whistle serves as a cue for song learning, enabling acquisition of normally rejected sounds of other species, including hermit thrush, Catharus guttatus, notes, which have a sound quality distinct from that of natural white-crowned sparrow phrases. Our results support the conclusion that sensory mechanisms rather than motor constraints are primarily responsible for the selectivity seen in song learning. Copyright 2000 The Association for the Study of Animal Behaviour.     

A Potential Metric of the Attractiveness of Bird Song to Humans

The prevalence of passerines (mostly oscines, or songbirds) in international bird trade suggests that the possession or production of a song that is attractive or desirable to people may contribute to the likelihood of a species being traded. Testing this is difficult because we lack a general and readily available metric that quantifies attractiveness of bird song to humans. We propose and validate such a metric, based on the number of sound files lodged for a species on the Xeno‐Canto website ( www.xeno-canto.org ). Our hypothesis is that species with more attractive songs are likely to be recorded more often, and so be represented more often in this online bird sound resource, all else being equal. Using a sample of North American and European passerines, we show that song repertoire size and geographic range size are consistently related to the number of recordings on Xeno‐Canto. We use these results to derive a metric (the residuals of a model of the number of recordings in Xeno‐Canto as a function of geographic range size) that may identify songs that are attractive to humans. Bird species whose songs are known to have inspired classical music, including several well known for their songs (e.g. common nightingale, European blackbird), have higher values of the metric than those that have not been referenced in classical music. The metric may help explain which bird species are present in trade, and so contribute to studies of invasion and conservation biology.     

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.     

Neural correlates of learned song in the avian forebrain: simultaneous representation of self and others

Songbirds are extraordinary vocalists and sensitive listeners, singing to communicate identity, engage other birds in acoustical combat, and attract mates. These processes involve auditory plasticity in that birds rapidly learn to discriminate novel from familiar songs. Songbirds also are one of the few non-human animals that use auditory feedback to learn their vocalizations, thus auditory -- vocal interactions are likely to be important to vocal learning. Recent advances strengthen the connection between song recognition and processing of birdsong in the auditory telencephalon. New insights also have emerged into the mechanisms underlying the 'gating' of auditory responses and the emergence of highly selective responses, two processes that could facilitate auditory feedback important to song learning.     

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.     

The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata)

Vocal acquisition in songbirds and humans shows many similarities, one of which is that both involve a combination of experience and perceptual predispositions. Among languages some speech sounds are shared, while others are not. This could reflect a predisposition in young infants for learning some speech sounds over others, which combines with exposure-based learning. Similarly, in songbirds, some sounds are common across populations, while others are more specific to populations or individuals. We examine whether this is also due to perceptual preferences for certain within-species element types in naive juvenile male birds, and how such preferences interact with exposure to guide subsequent song learning. We show that young zebra finches lacking previous song exposure perceptually prefer songs with more common zebra finch song element types over songs with less common elements. Next, we demonstrate that after subsequent tutoring, birds prefer tutor songs regardless of whether these contain more common or less common elements. In adulthood, birds tutored with more common elements showed a higher song similarity to their tutor song, indicating that the early bias influenced song learning. Our findings help to understand the maintenance of similarities and the presence of differences among birds'' songs, their dialects and human languages.     

Context-dependent vocal mimicry in a passerine bird

How do birds select the sounds they mimic, and in what contexts do they use vocal mimicry? Some birds show a preference for mimicking other species' alarm notes, especially in situations when they appear to be alarmed. Yet no study has demonstrated that birds change the call types they mimic with changing contexts. We found that greater racket-tailed drongos (Dicrurus paradiseus) in the rainforest of Sri Lanka mimic the calls of predators and the alarm-associated calls of other species more often than would be expected from the frequency of these sounds in the acoustic environment. Drongos include this alarm-associated mimicry in their own alarm vocalizations, while incorporating other species' songs and contact calls in their own songs. Drongos show an additional level of context specificity by mimicking other species' ground predator-specific call types when mobbing. We suggest that drongos learn other species' calls and their contexts while interacting with these species in mixed flocks. The drongos' behaviour demonstrates that alarm-associated calls can have learned components, and that birds can learn the appropriate usage of calls that encode different types of information.     

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.     

Recurring patterns in the songs of humpback whales (Megaptera novaeangliae)

Humpback whales, unlike most mammalian species, learn new songs as adults. Populations of singers progressively and collectively change the sounds and patterns within their songs throughout their lives and across generations. In this study, humpback whale songs recorded in Hawaii from 1985 to 1995 were analyzed using self-organizing maps (SOMs) to classify the sounds within songs, and to identify sound patterns that were present across multiple years. These analyses supported the hypothesis that recurring, persistent patterns exist within whale songs, and that these patterns are defined at least in part by acoustic relationships between adjacent sounds within songs. Sound classification based on acoustic differences between adjacent sounds yielded patterns within songs that were more consistent from year to year than classifications based on the properties of single sounds. Maintenance of fixed ratios of acoustic modulation across sounds, despite large variations in individual sounds, suggests intrinsic constraints on how sounds change within songs. Such acoustically invariant cues may enable whales to recognize and assess variations in songs despite propagation-related distortion of individual sounds and yearly changes in songs.     

Effects of auditory stimuli on the lifespan of Drosophila melanogaster

It is well known that music can have calming effects on humans, other mammals and birds. Reducing environmental stress or enhancing the resistance to certain stressors has been shown to extend lifespan in several organisms. Evidence also suggests that mild temporary stress may also enhance stress resistance and ultimately slow the aging process. This study explored the possibility that music may influence the lifespan of the fruit fly Drosophila melanogaster, possibly by affecting responses to stress. Flies received either background sounds (control), or background sounds supplemented with music (experimental). The experimental group had classical music playing constantly at an average of 20 dB above background sound. The median lifespan of females receiving music was 42 days compared to the median of 45 days without music, but the difference was not significant. For males median lifespans were 42 days with music exposure, and 47 days without music and the difference was significant. These results suggest that exposure to classical music decreased the lifespan of male Drosophila. Both experimental and control populations showed age-dependent increases in mortality, indicating that music affects the normal aging process rather than showing overt toxicity. These results suggest that certain auditory stimuli may be stressful and can be used as insect management.