Anthropogenic noise decreases urban songbird diversity and may contribute to homogenization

More humans reside in urban areas than at any other time in history. Protected urban green spaces and transportation greenbelts support many species, but diversity in these areas is generally lower than in undeveloped landscapes. Habitat degradation and fragmentation contribute to lowered diversity and urban homogenization, but less is known about the role of anthropogenic noise. Songbirds are especially vulnerable to anthropogenic noise because they rely on acoustic signals for communication. Recent studies suggest that anthropogenic noise reduces the density and reproductive success of some bird species, but that species which vocalize at frequencies above those of anthropogenic noise are more likely to inhabit noisy areas. We hypothesize that anthropogenic noise is contributing to declines in urban diversity by reducing the abundance of select species in noisy areas, and that species with low‐frequency songs are those most likely to be affected. To examine this relationship, we calculated the noise‐associated change in overall species richness and in abundance for seven common songbird species. After accounting for variance due to vegetative differences, species richness and the abundance of three of seven species were reduced in noisier locations. Acoustic analysis revealed that minimum song frequency was highly predictive of a species' response to noise, with lower minimum song frequencies incurring greater noise‐associated reduction in abundance. These results suggest that anthropogenic noise affects some species independently of vegetative conditions, exacerbating the exclusion of some songbird species in otherwise suitable habitat. Minimum song frequency may provide a useful metric to predict how particular species will be affected by noise. In sum, mitigation of noise may enhance habitat suitability for many songbird species, especially for species with songs that include low‐frequency elements.     

Urban noise and the cultural evolution of bird songs

In urban environments, anthropogenic noise can interfere with animal communication. Here we study the influence of urban noise on the cultural evolution of bird songs. We studied three adjacent dialects of white-crowned sparrow songs over a 30-year time span. Urban noise, which is louder at low frequencies, increased during our study period and therefore should have created a selection pressure for songs with higher frequencies. We found that the minimum frequency of songs increased both within and between dialects during the 30-year time span. For example, the dialect with the highest minimum frequency is in the process of replacing another dialect that has lower frequency songs. Songs with the highest minimum frequency were favoured in this environment and should have the most effective transmission properties. We suggest that one mechanism that influences how dialects, and cultural traits in general, are selected and transmitted from one generation to the next is the dialect''s ability to be effectively communicated in the local environment.     

Black‐capped chickadees Poecile atricapillus sing at higher pitches with elevated anthropogenic noise,but not with decreasing canopy cover

Several songbird species sing at higher frequencies (i.e. higher pitch) when anthropogenic noise levels are elevated. Such frequency shifting is thought to be an adaptation to prevent masking of bird song by anthropogenic noise. However, no study of this phenomenon has examined how vegetative differences between noisy and quiet sites influence frequency shifting. Variation in vegetative structure is important because the acoustic adaptation hypothesis predicts that birds in more open areas should also sing at higher frequencies. Thus, vegetative structure may partially explain the observation of higher frequency songs in areas with high levels of anthropogenic noise. To distinguish between frequency shifting due to noise or vegetative structure we recorded the songs of black‐capped chickadees Poecile atricapillus vocalizing in high and low noise sites with open and closed canopy forests. Consistent with the noise‐dependent frequency hypothesis, black‐capped chickadees sang at higher frequencies in high noise sites than in low noise sites. In contrast, birds did not sing at higher frequencies in sites with more open canopies. These results suggest that frequency shifting in chickadees is more strongly related to ambient noise levels than to vegetative structure. A second frequency measure, inter‐note ratio, was reduced at higher levels of canopy cover. We speculate that this may be due to a non‐random distribution of dominant males. In sum, our results support the hypothesis that some birds sing at higher frequencies to avoid overlap with anthropogenic noise, but suggest that vegetative structure may play a role in the modification of other song traits.     

Acoustic adaptations to anthropogenic noise in the cicada Cryptotympana takasagona Kato (Hemiptera: Cicadidae)

Anthropogenic noise produced by human activities affects acoustic communication in animals living in urban habitats. We recorded the calling songs of the cicada Cryptotympana takasagona in the Kaohsiung metropolitan areas of southern Taiwan to investigate possible acoustic adaptations to anthropogenic noise. C. takasagona did not call more in noise gaps. Acoustic features (peak frequency, quartile 25%, quartile 50%, and quartile 75%) of calling songs significantly increased with ambient noise levels. C. takasagona shifted the energy distribution of calling songs to higher frequencies in the presence of higher noise levels. We suggest that the acoustic adaptation by which song frequencies increase with levels of anthropogenic noise in C. takasagona may result from a size-dependent calling strategy in which small-sized males call more in noise conditions or large-sized males adjust their song frequency by changing their abdominal cavities.     

House Wrens Troglodytes aedon reduce repertoire size and change song element frequencies in response to anthropogenic noise

Anthropogenic noise (≤ 3 kHz) can affect key features of birds’ acoustic communication via two different processes: (1) song‐learning, because songbirds need to hear themselves and other birds to crystallize their song, and (2) avoidance of song elements that overlap with anthropogenic noise. In this study we tested whether anthropogenic noise reduces the number of song elements in the repertoire of House Wren Troglodytes aedon, an urban species. Additionally, we tested whether the proportion of high‐frequency elements (i.e. elements where the minimum frequency is above 3 kHz) is related to anthropogenic noise levels, and how the frequencies and duration of shared elements between males change with different levels of anthropogenic noise. We recorded 29 House Wren males exposed to different anthropogenic noise levels (36.50–79.50 dB) during two consecutive breeding seasons from four locations. We recorded each male on 2 days during each season continuously for 50 min (we collected 104 h of recordings) and measured anthropogenic noise levels every 10 min inside each male territory during the recording period. In general, individuals inhabiting noisier territories had smaller repertoires. However, only in two locations with anthropogenic noise levels between 38.60 and 79.50 dB did males inhabiting noisier territories have smaller repertoires. In the other two locations with lower anthropogenic noise (36.50–66.50 dB), the anthropogenic noise inside each territory was not related to the repertoire size. Individuals inhabiting the noisiest location showed a tendency to include more high‐frequency elements in their songs. In 26% of the elements, the anthropogenic noise affected their frequency features. Our results showed that not all House Wrens inhabiting urban environments modify their songs at the highest level of organization (i.e. repertoire) to reduce the masking effect of anthropogenic noise on acoustic communication.     

Song characteristics track bill morphology along a gradient of urbanization in house finches (<Emphasis Type="Italic">Haemorhous mexicanus</Emphasis>)

Introduction

Urbanization can considerably impact animal ecology, evolution, and behavior. Among the new conditions that animals experience in cities is anthropogenic noise, which can limit the sound space available for animals to communicate using acoustic signals. Some urban bird species increase their song frequencies so that they can be heard above low-frequency background city noise. However, the ability to make such song modifications may be constrained by several morphological factors, including bill gape, size, and shape, thereby limiting the degree to which certain species can vocally adapt to urban settings. We examined the relationship between song characteristics and bill morphology in a species (the house finch, Haemorhous mexicanus) where both vocal performance and bill size are known to differ between city and rural animals.

Results

We found that bills were longer and narrower in more disturbed, urban areas. We observed an increase in minimum song frequency of urban birds, and we also found that the upper frequency limit of songs decreased in direct relation to bill morphology.

Conclusions

These findings are consistent with the hypothesis that birds with longer beaks and therefore longer vocal tracts sing songs with lower maximum frequencies because longer tubes have lower-frequency resonances. Thus, for the first time, we reveal dual constraints (one biotic, one abiotic) on the song frequency range of urban animals. Urban foraging pressures may additionally interact with the acoustic environment to shape bill traits and vocal performance.

     

Degradation of rural and urban great tit song: testing transmission efficiency

Acoustic signals play a fundamental role in avian territory defence and mate attraction. Several studies have now shown that spectral properties of bird song differ between urban and rural environments. Previously this has been attributed to competition for acoustic space as a result of low-frequency noise present in cities. However, the physical structure of urban areas may have a contributory effect. Here we investigate the sound degradation properties of woodland and city environments using both urban and rural great tit song. We show that although urban surroundings caused significantly less degradation to both songs, the transmission efficiency of rural song compared to urban song was significantly lower in the city. While differences between the two songs in woodland were generally minimal, some measures of the transmission efficiency of rural song were significantly lower than those of urban song, suggesting additional benefits to singing rural songs in this setting. In an attempt to create artificial urban song, we mimicked the increase in minimum frequency found several times previously in urban song. However, this did not replicate the same transmission properties as true urban song, suggesting changes in other song characteristics, such as temporal adjustments, are needed to further increase transmission of an avian signal in the city. We suggest that the structure of the acoustic environment, in addition to the background noise, plays an important role in signal adaptation.     

Urban noise influences vocalization structure in the House Wren Troglodytes aedon

Urban habitats are noisy and constrain acoustic communication in birds. We analysed the effect of anthropogenic noise on the vocalization characteristics of House Wrens Troglodytes aedon at two sites with different noise levels (rural and urban). We measured in each song and song trill the frequency bandwidth, maximum amplitude, highest and minimum frequency, and trill rate. In noisy urban environments, there was a reduction in bandwidth and an increase in trill rate relative to quieter, rural environments. The whole song of birds from both populations increased in minimum frequency as noise increased, improving song transmission.     

White‐crowned sparrow males show immediate flexibility in song amplitude but not in song minimum frequency in response to changes in noise levels in the field

The soundscape acts as a selective agent on organisms that use acoustic signals to communicate. A number of studies document variation in structure, amplitude, or timing of signal production in correspondence with environmental noise levels thus supporting the hypothesis that organisms are changing their signaling behaviors to avoid masking. The time scale at which organisms respond is of particular interest. Signal structure may evolve across generations through processes such as cultural or genetic transmission. Individuals may also change their behavior during development (ontogenetic change) or in real time (i.e., immediate flexibility). These are not mutually exclusive mechanisms, and all must be investigated to understand how organisms respond to selection pressures from the soundscape. Previous work on white‐crowned sparrows (Zonotrichia leucophrys) found that males holding territories in louder areas tend to sing higher frequency songs and that both noise levels and song frequency have increased over time (30 years) in urban areas. These previous findings suggest that songs are changing across generations; however, it is not known if this species also exhibits immediate flexibility. Here, we conducted an exploratory, observational study to ask whether males change the minimum frequency of their song in response to immediate changes in noise levels. We also ask whether males sing louder, as increased minimum frequency may be physiologically linked to producing sound at higher amplitudes, in response to immediate changes in environmental noise. We found that territorial males adjust song amplitude but not minimum frequency in response to changes in environmental noise levels. Our results suggest that males do not show immediate flexibility in song minimum frequency, although experimental manipulations are needed to test this hypothesis further. Our work highlights the need to investigate multiple mechanisms of adaptive response to soundscapes.     

Exposure to noise pollution across North American passerines supports the noise filter hypothesis

The noise filter hypothesis predicts that species using higher sound frequencies should be more tolerant of noise pollution, because anthropogenic noise is more intense at low frequencies. Recent work analysed continental‐scale data on anthropogenic noise across the USA and found that passerine species inhabiting more noise‐polluted areas do not have higher peak song frequency but have more complex songs. However, this metric of song complexity is of ambiguous interpretation, because it can indicate either diverse syllables or a larger frequency bandwidth. In the latter case, the finding would support the noise filter hypothesis, because larger frequency bandwidths mean that more sound energy spreads to frequencies that are less masked by anthropogenic noise. We reanalysed how passerine song predicts exposure to noise using a more thorough dataset of acoustic song measurements, and showed that it is large frequency bandwidths, rather than diverse syllables, that predict the exposure of species to noise pollution. Given that larger bandwidths often encompass higher maximum frequencies, which are less masked by anthropogenic noise, our result suggests that tolerance to noise pollution might depend mostly on having the high‐frequency parts of song little masked by noise, thus preventing acoustic communication from going entirely unnoticed at long distances.     

城市噪声使树麻雀鸣唱的最低频率升高

随着城市化进程的不断加快,城市噪声水平显著升高。噪声会掩盖鸟类的声音信号,这无疑会影响鸟类的交流。在嘈杂的城市环境中,鸟类通常以高频率鸣唱来避免声信号被掩蔽。然而,较低的发声频率才是雄性品质的重要表征,提高发声频率可能会影响声信号对雌性的吸引力。因此,鸟类会在提高发声频率和保持较低频率之间进行权衡。为确定城市噪声对树麻雀（Passer montanus）鸣唱行为的影响,在沈阳市选取6个研究地点,比较了沈阳市区和近郊不同噪声水平下树麻雀繁殖期的鸣唱特征。在2019年4月至7月,使用定向麦克风录制了320只繁殖期树麻雀的鸣唱,并使用声级计测定噪声水平。研究结果显示,城市研究地点的噪声水平显著高于郊区研究地点。与安静郊区相比,城市嘈杂环境中的树麻雀鸣唱的最高频率、最低频率和主峰峰频显著较高,频宽更大,而时长没有差别。树麻雀鸣唱的最高频率、频宽、主峰峰频和时长均与噪声水平无显著相关,而最低频率与研究地点的噪声水平呈显著正相关。上述结果说明,在噪声环境中,树麻雀选择提高最低频率以利于声信号的传输。     

Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals

Abstract.— Bird song is a sexual trait important in mate choice and known to be shaped by environmental selection. Here we investigate the ecological factors shaping song variation across a rainforest gradient in central Africa. We show that the little greenbul ( Andropadus virens ), previously shown to vary morphologically across the gradient in fitness-related characters, also varies with respect to song characteristics. Acoustic features, including minimum and maximum frequency, and delivery rate of song notes showed significant differences between habitats. In contrast, we found dialectal variation independent of habitat in population-typical songtype sequences. This pattern is consistent with ongoing gene flow across habitats and in line with the view that song variation in the order in which songtypes are produced is not dependent on habitat characteristics in the same way physical song characteristics are. Sound transmission characteristics of the two habitats did not vary significantly, but analyses of ambient noise spectra revealed dramatic and consistent habitat-dependent differences. Matching between low ambient noise levels for low frequencies in the rainforest and lower minimal frequencies in greenbul songs in this habitat suggests that part of the song divergence may be driven by habitat-dependent ambient noise patterns. These results suggest that habitat-dependent selection may act simultaneously on traits of ecological importance and those important in prezygotic isolation, leading to an association between morphological and acoustic divergence. Such an association may promote assortative mating and may be a mechanism driving reproductive divergence across ecological gradients.     

Flexibility in animal signals facilitates adaptation to rapidly changing environments

Charles Darwin posited that secondary sexual characteristics result from competition to attract mates. In male songbirds, specialized vocalizations represent secondary sexual characteristics of particular importance because females prefer songs at specific frequencies, amplitudes, and duration. For birds living in human-dominated landscapes, historic selection for song characteristics that convey fitness may compete with novel selective pressures from anthropogenic noise. Here we show that black-capped chickadees (Poecile atricapillus) use shorter, higher-frequency songs when traffic noise is high, and longer, lower-frequency songs when noise abates. We suggest that chickadees balance opposing selective pressures by use low-frequency songs to preserve vocal characteristics of dominance that repel competitors and attract females, and high frequency songs to increase song transmission when their environment is noisy. The remarkable vocal flexibility exhibited by chickadees may be one reason that they thrive in urban environments, and such flexibility may also support subsequent genetic adaptation to an increasingly urbanized world.     

Negative impact of urban noise on sexual receptivity and clutch size in female domestic canaries

In oscines, male song stimulates female reproduction and females are known to adjust both their sexual preferences and their maternal investment according to song quality. Female domestic canaries are especially responsive to wide frequency bandwidth (4 kHz) male songs emitted with a high‐repetition syllable rate and low minimal frequencies (1 kHz). We previously showed that low‐frequency urban noise decreases female sexual responsiveness for these low‐frequency songs (1–5 kHz) through auditory masking. Based on the differential allocation hypothesis, we predicted that urban noise exposure will equally affect female maternal investment. Using a crossover design, we broadcast low‐frequency songs to females either in an overlapping noise condition or in an alternating noise condition. Females decreased both their sexual responsiveness and their clutch size in the overlapping noise treatment relative to the alternative noise treatment. No differences were found concerning egg size or egg composition (yolk and albumen mass, testosterone concentration). Due to our experimental design, we can exclude a general impact of noisy conditions and thereby provide evidence for a detrimental effect through masking on avian courtship and reproductive output. These results suggest that noisy conditions may also affect avian communication in outdoor conditions, which may partly explain field reports on noise‐dependent breeding success and reduced breeding densities at noisy sites.     

Effects of urban noise on song and response behaviour in great tits

Acoustic communication is fundamental in avian territory defence and mate attraction. In urban environments where sound transmissions are more likely to be masked by low-frequency anthropogenic noise, acoustic adaptations may be advantageous. However, minor modifications to a signal could affect its efficacy. While recent research has shown that there is divergence between songs from noisy and quiet areas, it is unknown whether these differences affect the response to the signal by its receivers. Here, we show that there is a difference in spectral aspects of rural and urban song in a common passerine, the great tit Parus major, at 20 sites across the UK. We also provide, to our knowledge, the first demonstration that such environmentally induced differences in song influence the response of male territory holders. Males from quiet territories exhibited a significantly stronger response when hearing song from another territory holder with low background noise than from those with high background noise. The opposite distinction in response intensity to homotypic versus heterotypic song was observed in males from noisy territories. This behavioural difference may intensify further signal divergence between urban and rural populations and raises important questions concerning signal evolution.     

Different behavioural responses to anthropogenic noise by two closely related passerine birds

Anthropogenic noise, now common to many landscapes, can impair acoustic communication for many species, yet some birds compensate for masking by noise by altering their songs. The phylogenetic distribution of these noise-dependent signal adjustments is uncertain, and it is not known whether closely related species respond similarly to noise. Here, we investigated the influence of noise on habitat occupancy rates and vocal frequency in two congeneric vireos with similar song features. Noise exposure did not influence occupancy rates for either species, yet song features of both changed, albeit in different ways. With increases in noise levels, plumbeous vireos (Vireo plumbeus) sang shorter songs with higher minimum frequencies. By contrast, grey vireos (Vireo vicinior) sang longer songs with higher maximum frequencies. These findings support the notion that vocal plasticity may help some species occupy noisy areas, but because there were no commonalities among the signal changes exhibited by these closely related birds, it may be difficult to predict how diverse species may modify their signals in an increasingly noisy world.     

Variation in adrenocortical stress physiology and condition metrics within a heterogeneous urban environment in the song sparrow Melospiza melodia

In urban habitats, organisms face unique fitness challenges including disturbance from human activity and noise. One physiological mechanism that may be plastically or evolutionarily modified to ameliorate deleterious effects of anthropogenic disturbance is the adrenocortical stress response. Individuals in urban environments may display smaller stress responses, which may prevent pathologies associated with consistent elevation of stress hormones, and may also show differences in baseline corticosterone (CORT, the primary avian stress hormone), due to altered energetic demands or chronic stress. We examined whether stress physiology and condition metrics in male song sparrows Melospiza melodia vary as a function of discrete differences in anthropogenic disturbance level (activity centers and refuges) or with continuous variation in an urbanization score and noise environment. Males breeding in activity centers displayed lower maximal (acute) CORT levels than activity refuge males, and acute CORT also tended to negatively correlate with urbanization score. Baseline CORT did not differ between habitat types, and activity center males also showed no evidence of changes in body mass, hematocrit, or antioxidant capacity. Further, activity center males had higher quality feathers (indicative of higher condition at molt) than activity refuge males. We found no indication that the noise environment altered stress physiology or condition in song sparrows. Overall, results suggest that song sparrows are an urban adapter species, which are not detrimentally affected by unique selective pressures encountered in the urban environment.     

Song convergence in multiple urban populations of silvereyes (Zosterops lateralis)

Recent studies have revealed differences between urban and rural vocalizations of numerous bird species. These differences include frequency shifts, amplitude shifts, altered song speed, and selective meme use. If particular memes sung by urban populations are adapted to the urban soundscape, "urban-typical" calls, memes, or repertoires should be consistently used in multiple urban populations of the same species, regardless of geographic location. We tested whether songs or contact calls of silvereyes (Zosterops lateralis) might be subject to such convergent cultural evolution by comparing syllable repertoires of geographically dispersed urban and rural population pairs throughout southeastern Australia. Despite frequency and tempo differences between urban and rural calls, call repertoires were similar between habitat types. However, certain song syllables were used more frequently by birds from urban than rural populations. Partial redundancy analysis revealed that both geographic location and habitat characteristics were important predictors of syllable repertoire composition. These findings suggest convergent cultural evolution: urban populations modify both song and call syllables from their local repertoire in response to noise.     

Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird

Research has shown that bird songs are modified in different ways to deal with urban noise and promote signal transmission through noisy environments. Urban noise is composed of low frequencies, thus the observation that songs have a higher minimum frequency in noisy places suggests this is a way of avoiding noise masking. Most studies are correlative and there is as yet little experimental evidence that this is a short-term mechanism owing to individual plasticity. Here we experimentally test if house finches (Carpodacus mexicanus) can modulate the minimum frequency of their songs in response to different noise levels. We exposed singing males to three continuous treatments: low–high–low noise levels. We found a significant increase in minimum frequency from low to high and a decrement from high to low treatments. We also found that this was mostly achieved by modifying the frequency of the same low-frequency syllable types used in the different treatments. When different low-frequency syllables were used, those sung during the noisy condition were longer than the ones sang during the quiet condition. We conclude that house finches modify their songs in several ways in response to urban noise, thus providing evidence of a short-term acoustic adaptation.     

Geographically pervasive effects of urban noise on frequency and syllable rate of songs and calls in silvereyes (Zosterops lateralis)

Recent studies in the Northern Hemisphere have shown that songbirds living in noisy urban environments sing at higher frequencies than their rural counterparts. However, several aspects of this phenomenon remain poorly understood. These include the geographical scale over which such patterns occur (most studies have compared local populations), and whether they involve phenotypic plasticity or microevolutionary change. We conducted a field study of silvereye (Zosterops lateralis) vocalizations over more than 1 million km(2) of urban and rural south-eastern Australia, and compared possible effects of urban noise on songs (which are learned) and contact calls (which are innate). Across 14 paired urban and rural populations, silvereyes consistently sang both songs and contact calls at higher frequencies in urban environments. Syllable rate (syllables per second) decreased in urban environments, consistent with the hypothesis that reflective structures degrade song and encourage longer intervals between syllables. This comprehensive study is, to our knowledge, the first to demonstrate varied adaptations of urban bird vocalizations over a vast geographical area, and to provide insight into the mechanism responsible for these changes.