Traffic noise disrupts vocal development and suppresses immune function.

Noise pollution has been linked to learning and language deficits in children, but the causal mechanisms connecting noise to cognitive deficiencies remain unclear because experimental models are lacking. Here, we investigated the effects of noise on birdsong learning, the primary animal model for vocal learning and speech development in humans. We found that traffic noise exposure retarded vocal development and led to learning inaccuracies. In addition, noise suppressed immune function during the sensitive learning period, indicating that it is a potent stressor for birds, which is likely to compromise their cognitive functions. Our results provide important insights into the consequences of noise pollution and pave the way for future studies using birdsong as an experimental model for the investigation of noise-induced learning impairments.

Traffic noise exposure depresses plasma corticosterone and delays offspring growth in breeding zebra finches.

The impact of human activity on the acoustic environment is overwhelming, with anthropogenic noise reaching even remote areas of the planet. The World Health Organization has identified noise pollution as one of the leading environmental health risks in humans, and it has been linked to a myriad of short- and long-term health effects in exposed individuals. However, less is known about the health effects of anthropogenic noise exposure on animals. We investigated long- and short-term effects of traffic noise on zebra finches breeding in small communal aviaries, using a repeated measures design. Birds bred in both noise and no-noise conditions, and we measured baseline plasma glucocorticoid levels before, during and after breeding. In addition, we assayed immune function, measured reproductive success and offspring growth and compared rates of extra-pair paternity of breeding adults. Breeding birds had significantly lower baseline plasma corticosterone levels when exposed to traffic noise than when they were not exposed to noise playback. In addition, the nestlings reared during noise exposure were lighter than nestlings of the same parents when breeding in control conditions. Our results suggest that traffic noise poses a more severe hurdle to birds at more vulnerable stages of their life history, such as during reproductive events and ontogeny. While chronic exposure to traffic noise in our birds did not, by itself, prove to be a sufficient stressor to cause acute effects on health or reproductive success in exposed individuals, it did result in disruptions to normal glucocorticoid profiles and delayed offspring growth. However, animals living in urban habitats are exposed to a multitude of anthropogenic disturbances, and it is likely that even species that appear to be thriving in noisy environments may suffer cumulative effects of these multiple disturbances that may together impact their fitness in urban environments.

Higher songs of city birds may not be an individual response to noise.

It has been observed in many songbird species that populations in noisy urban areas sing with a higher minimum frequency than do matched populations in quieter, less developed areas. However, why and how this divergence occurs is not yet understood. We experimentally tested whether chronic noise exposure during vocal learning results in songs with higher minimum frequencies in great tits (Parus major), the first species for which a correlation between anthropogenic noise and song frequency was observed. We also tested vocal plasticity of adult great tits in response to changing background noise levels by measuring song frequency and amplitude as we changed noise conditions. We show that noise exposure during ontogeny did not result in songs with higher minimum frequencies. In addition, we found that adult birds did not make any frequency or song usage adjustments when their background noise conditions were changed after song crystallization. These results challenge the common view of vocal adjustments by city birds, as they suggest that either noise itself is not the causal force driving the divergence of song frequency between urban and forest populations, or that noise induces population-wide changes over a time scale of several generations rather than causing changes in individual behaviour.

Vocal plasticity in a reptile.

Sophisticated vocal communication systems of birds and mammals, including human speech, are characterized by a high degree of plasticity in which signals are individually adjusted in response to changes in the environment. Here, we present, to our knowledge, the first evidence for vocal plasticity in a reptile. Like birds and mammals, tokay geckos (Gekko gecko) increased the duration of brief call notes in the presence of broadcast noise compared to quiet conditions, a behaviour that facilitates signal detection by receivers. By contrast, they did not adjust the amplitudes of their call syllables in noise (the Lombard effect), which is in line with the hypothesis that the Lombard effect has evolved independently in birds and mammals. However, the geckos used a different strategy to increase signal-to-noise ratios: instead of increasing the amplitude of a given call type when exposed to noise, the subjects produced more high-amplitude syllable types from their repertoire. Our findings demonstrate that reptile vocalizations are much more flexible than previously thought, including elaborate vocal plasticity that is also important for the complex signalling systems of birds and mammals. We suggest that signal detection constraints are one of the major forces driving the evolution of animal communication systems across different taxa.

Lombard effect onset times reveal the speed of vocal plasticity in a songbird.

Animals that use vocal signals to communicate often compensate for interference and masking from background noise by raising the amplitude of their vocalisations. This response has been termed the Lombard effect. However, despite more than a century of research, little is known how quickly animals can adjust the amplitude of their vocalisations after the onset of noise. The ability to respond quickly to increases in noise levels would allow animals to avoid signal masking and ensure their calls continue to be heard, even if they are interrupted by sudden bursts of high-amplitude noise. We tested how quickly singing male canaries (Serinus canaria) exhibit the Lombard effect by exposing them to short playbacks of white noise and measuring the speed of their responses. We show that canaries exhibit the Lombard effect in as little as 300 ms after the onset of noise and are also able to increase the amplitude of their songs mid-song and mid-phrase without pausing. Our results demonstrate high vocal plasticity in this species and suggest that birds are able to adjust the amplitude of their vocalisations very rapidly to ensure they can still be heard even during sudden changes in background noise levels.

Traffic noise drowns out great tit alarm calls.

Anthropogenic noise is one of the fastest growing and most ubiquitous types of environmental pollution and can impair acoustic communication in a variety of animals [1]. Recent research has shown that birds can adjust acoustic parameters of their sexual signals (songs) in noisy environments [2,3], yet we know little about other types of vocalizations. Anti-predator signals contain subtle information that is critical for avoiding predation [4,5], and failure to detect these calls [6,7] as a result of anthropogenic noise pollution could have large fitness consequences by negatively impacting survival. We investigated whether traffic noise impacts both the production and perception of avian alarm calls using a combination of lab and field experiments with great tits (Parus major), a songbird that frequently inhabits noise-polluted environments. In response to experimental noise manipulation in controlled laboratory conditions, great tits increased the amplitude, but not the frequency parameters, of their mobbing alarm calls (hereafter 'alarm calls'). Playback experiments conducted in the wild indicate that current levels of road traffic noise mask alarm calls, impeding the ability of great tits to perceive these critical signals. These results show that, despite the vocal adjustments used to compensate for anthropogenic noise, great tits are not able to restore the active space of their calls in even moderately noisy environments. Consequently, birds are likely to suffer from increased predation risk under noise, with likely effects on their behaviour, populations, and community dynamics in noise-polluted areas.

Bird song and anthropogenic noise: vocal constraints may explain why birds sing higher-frequency songs in cities.

When animals live in cities, they have to adjust their behaviour and life histories to novel environments. Noise pollution puts a severe constraint on vocal communication by interfering with the detection of acoustic signals. Recent studies show that city birds sing higher-frequency songs than their conspecifics in non-urban habitats. This has been interpreted as an adaptation to counteract masking by traffic noise. However, this notion is debated, for the observed frequency shifts seem to be less efficient at mitigating noise than singing louder, and it has been suggested that city birds might use particularly high-frequency song elements because they can be produced at higher amplitudes. Here, we present the first phonetogram for a songbird, which shows that frequency and amplitude are strongly positively correlated in the common blackbird (Turdus merula), a successful urban colonizer. Moreover, city blackbirds preferentially sang higher-frequency elements that can be produced at higher intensities and, at the same time, happen to be less masked in low-frequency traffic noise.

On the evolution of noise-dependent vocal plasticity in birds.

Signal plasticity is considered an important step in the evolution of animal communication. In acoustic communication, signal transmission is often constrained by background noise. One adaptation to evade acoustic signal masking is the Lombard effect, in which an animal increases its vocal amplitude in response to an increase in background noise. This form of signal plasticity has been found in mammals, including humans, and some birds, but not frogs. However, the evolution of the Lombard effect is still unclear. Here we demonstrate for the first time the Lombard effect in a phylogentically basal bird species, the tinamou Eudromia elegans. By doing so, we take a step towards reconstructing the evolutionary history of noise-dependent vocal plasticity in birds. Similar to humans, the tinamous also raised their vocal pitch in noise, irrespective of any release from signal masking. The occurrence of the Lombard effect in a basal bird group suggests that this form of vocal plasticity was present in the common ancestor of all living birds and thus evolved at least as early as 119 Ma.

Metabolic and respiratory costs of increasing song amplitude in zebra finches.

Bird song is a widely used model in the study of animal communication and sexual selection, and several song features have been shown to reflect the quality of the singer. Recent studies have demonstrated that song amplitude may be an honest signal of current condition in males and that females prefer high amplitude songs. In addition, birds raise the amplitude of their songs to communicate in noisy environments. Although it is generally assumed that louder song should be more costly to produce, there has been little empirical evidence to support this assumption. We tested the assumption by measuring oxygen consumption and respiratory patterns in adult male zebra finches (Taeniopygia guttata) singing at different amplitudes in different background noise conditions. As background noise levels increased, birds significantly increased the sound pressure level of their songs. We found that louder songs required significantly greater subsyringeal air sac pressure than quieter songs. Though increased pressure is probably achieved by increasing respiratory muscle activity, these increases did not correlate with measurable increases in oxygen consumption. In addition, we found that oxygen consumption increased in higher background noise, independent of singing behaviour. This observation supports previous research in mammals showing that high levels of environmental noise can induce physiological stress responses. While our study did not find that increasing vocal amplitude increased metabolic costs, further research is needed to determine whether there are other non-metabolic costs of singing louder or costs associated with chronic noise exposure.

Developmental stress affects song learning but not song complexity and vocal amplitude in zebra finches.

Several recent studies have tested the hypothesis that song quality in adult birds may reflect early developmental conditions, specifically nutritional stress during the nestling period. Whilst all of these earlier studies found apparent links between early nutritional stress and song quality, their results disagree as to which aspects of song learning or production were affected. In this study, we attempted to reconcile these apparently inconsistent results. Our study also provides the first assessment of song amplitude in relation to early developmental stress and as a potential cue to male quality. We used an experimental manipulation in which the seeds on which the birds were reared were mixed with husks, making them more difficult for the parents to obtain. Compared with controls, such chicks were lighter at fledging; they were thereafter placed on a normal diet and had caught up by 100 days. We show that nutritional stress during the first 30 days of life reduced the birds' accuracy of song syntax learning, resulting in poorer copies of tutor songs. Our experimental manipulations did not lead to significant changes in song amplitude, song duration or repertoire size. Thus, individual differences observed in song performance features probably reflect differences in current condition or motivation rather than past condition.

Two-voice complexity from a single side of the syrinx in northern mockingbird Mimus polyglottos vocalizations.

The diverse vocal signals of songbirds are produced by highly coordinated motor patterns of syringeal and respiratory muscles. These muscles control separate sound generators on the right and left side of the duplex vocal organ, the syrinx. Whereas most song is under active neural control, there has been a growing interest in a different class of nonlinear vocalizations consisting of frequency jumps, subharmonics, biphonation and deterministic chaos that are also present in the vocal repertoires of many vertebrates, including many birds. These nonlinear phenomena may not require active neural control, depending instead on the intrinsic nonlinear dynamics of the oscillators housed within each side of the syrinx. This study investigates the occurrence of these phenomena in the vocalizations of intact northern mockingbirds Mimus polyglottos. By monitoring respiratory pressure and airflow on each side of the syrinx, we provide the first analysis of the contribution made by each side of the syrinx to the production of nonlinear phenomena and are able to reliably discriminate two-voice vocalizations from potentially similar appearing, unilaterally produced, nonlinear events. We present the first evidence of syringeal lateralization of nonlinear dynamics during bilaterally produced chaotic calls. The occurrence of unilateral nonlinear events was not consistently correlated with fluctuations in air sac pressure or the rate of syringeal airflow. Our data support previous hypotheses for mechanical and acoustic coupling between the two sides of the syrinx. These results help lay a foundation upon which to understand the communicative functions of nonlinear phenomena.

Producing song: the vocal apparatus.

In order to achieve the goal of understanding the neurobiology of birdsong, it is necessary to understand the peripheral mechanisms by which song is produced. This paper reviews recent advances in the understanding of syringeal and respiratory motor control and how birds utilize these systems to create their species-typical sounds. Songbirds have a relatively homogeneous duplex vocal organ in which sound is generated by oscillation of a pair of thickened labia on either side of the syrinx. Multiple pairs of syringeal muscles provide flexible, independent control of sound frequency and amplitude, and each side of the syrinx exhibits a degree of acoustic specialization. This is in contrast to many non-songbirds, including vocal learners such as parrots, which have fewer syringeal muscles and use syringeal membranes to generate sound. In doves, at least, these membranes generate a harmonic signal in which the fundamental frequency is regulated by respiratory pressure in the air sac surrounding the syrinx and the overtones are filtered out by the vocal tract. The songs of adult songbirds are generally accompanied by precisely coordinated respiratory and syringeal motor patterns that, despite their relative stereotypy, are modulated in real time by somatosensory feedback. Comparative studies indicate songbirds have evolved species-specific motor patterns that utilize the two sides of the syrinx in specific ways and enhance the particular acoustic effects characterizing the species song. A vocal mimic tutored with heterospecific song uses the same motor pattern as the tutor species when he accurately copies the song, suggesting that physical or physiological constraints on sound production have had a prominent role in the evolution of species-specific motor patterns. An understanding of the relationship between the central processing and peripheral performance of song motor programs is essential for an understanding of the development, function, and evolution of these complex vocal signals.

Motor mechanisms of a vocal mimic: implications for birdsong production.

The diverse vocal performances of oscine songbirds are produced by the independent but coordinated patterns of activity in muscles controlling separate sound generators on the left and right sides of their duplex vocal organ, the syrinx. Species with different song styles use the two sides of their syrinx in different ways to produce their species-typical songs. Understanding how a vocal mimic copies another species' song may provide an insight into whether there are alternative motor mechanisms for generating the model's song and what parts of his song are most difficult to produce. We show here that when a vocal mimic, the northern mockingbird, accurately copies the song of another species it also uses the vocal motor pattern employed by the model species. Deviations from the model's production mechanism result in predictable differences in the mockingbird's song. Species-specific acoustic features of the model seem most difficult to copy, suggesting that they have been exposed to the strongest selective pressure to maximize their performance.