Wouter Halfwerk

A behavioural mechanism explaining noise-dependent frequency use in urban birdsong

Acoustic signals are usually very effective in long-distance communication. However, in many habitats animals suffer more and more from signal interference caused by traffic-generated low-frequency noise. Recent observations suggest that birds are able to change the pitch of their song to reduce masking interference, but we still lack experimental evidence. Theoretically, some bird species, when confronted with increased noise levels, may be able to switch to song types in their repertoire with higher frequencies. We tested this hypothesis in the great tit, Parus major, by exposing singing males to low-frequency ‘city’ noise in their natural territories and comparing frequency characteristics of songs before and after song type switching. We also exposed birds to high-frequency, ‘inverse’ city noise, as well as to white noise as a control. Great tits adjusted temporal switching behaviour in response to noise exposure. Song types that were less masked by the noise treatment were sung for longer durations. As a result, all five birds that switched during the low-frequency noise treatment switched to song types with a higher minimum frequency. Similarly, seven of nine birds that switched while exposed to high-frequency noise switched to song types with lower maximum frequencies. These results provide experimental evidence for a short-term behavioural mechanism explaining noise-dependent frequency use in birdsong.

Low-frequency songs lose their potency in noisy urban conditions

Many animal species communicate with their mates through acoustic signals, but this communication seems to become a struggle in urbanized areas because of increasing anthropogenic noise levels. Several bird species have been reported to increase song frequency by which they reduce the masking impact of spectrally overlapping noise. However, it remains unclear whether such behavioral flexibility provides a sufficient solution to noisy urban conditions or whether there are hidden costs. Species may rely on low frequencies to attract and impress females, and the use of high frequencies may, therefore, come at the cost of reduced attractiveness. We studied the potential tradeoff between signal strength and signal detection in a successful urban bird species, the great tit (Parus major). We show that the use of low-frequency songs by males is related to female fertility as well as sexual fidelity. We experimentally show that urban noise conditions impair male–female communication and that signal efficiency depends on song frequency in the presence of noise. Our data reveal a response advantage for high-frequency songs during sexual signaling in noisy conditions, whereas low-frequency songs are likely to be preferred. These data are critical for our understanding of the impact of anthropogenic noise on wild-ranging birds, because they provide evidence for low-frequency songs being linked to reproductive success and to be affected by noise-dependent signal efficiency.

SONG DIVERGENCE BY SENSORY DRIVE IN AMAZONIAN BIRDS

Visual signals are shaped by variation in the signaling environment through a process termed sensory drive, sometimes leading to speciation. However, the evidence for sensory drive in acoustic signals is restricted to comparisons between highly dissimilar habitats, or single‐species studies in which it is difficult to rule out the influence of undetected ecological variables, pleiotropic effects, or chance. Here we assess whether this form of sensory drive—often termed “acoustic adaptation”—can generate signal divergence across ecological gradients. By studying avian communities in two Amazonian forest types, we show that songs of 17 “bamboo‐specialist” bird species differ in predictable ways from their nearest relatives in adjacent terra firme forest. We also demonstrate that the direction of song divergence is correlated with the sound transmission properties of habitats, rather than with genetic divergence, ambient noise, or pleiotropic effects of mass and bill size. Our findings indicate that acoustic adaptation adds significantly to stochastic processes underlying song divergence, even when comparing between habitats with relatively similar structure. Furthermore, given that song differences potentially contribute to reproductive isolation, these findings are consistent with a wider role for sensory drive in the diversification of lineages with acoustic mating signals.

Habitat‐dependent song divergence at subspecies level in the grey‐breasted wood‐wren

Song divergence among populations can theoretically lead to reproductive divergence and speciation. Despite many studies, this theory is still controversial. Habitat differences have been shown to shape songs, but few studies have looked for a link between ecologically driven acoustic and genetic divergence. We tested whether environmental selection has driven song divergence in two genetically distinct, but hybridizing, subspecies of the grey‐breasted wood‐wren (Henicorhina leucophrys) in Ecuador. Several acoustic features showed significant divergence between the subspecies. Spectral song divergence correlated with ambient noise profiles which differed significantly between the habitats of both subspecies. Temporal song divergence also corresponded as expected to vegetation density. However, in terms of quantified levels of reverberations, we found no significant differences in habitat‐dependent sound transmission properties. We conclude that ecological niche segregation may explain acoustic divergence among the two wren subspecies. The resulting habitat‐dependent song divergence may have contributed to reproductive divergence by guiding assortative mating in parapatric conditions or just currently contribute to maintenance of reproductive isolation upon secondary contact.

ASYMMETRIC RESPONSE PATTERNS TO SUBSPECIES-SPECIFIC SONG DIFFERENCES IN ALLOPATRY AND PARAPATRY IN THE GRAY-BREASTED WOOD-WREN

Song divergence between closely related taxa may play a critical role in the evolutionary processes of speciation and hybridization. We explored song variation between two Ecuadorian subspecies of the gray‐breasted wood‐wren (Henicorhina leucophrys) and tested the impact of song divergence on response behaviors. Songs were significantly different between the two subspecies, even between two parapatric populations 10 km apart. Playback experiments revealed an asymmetric response pattern to these divergent subspecies specific songs; one subspecies responded more to songs of its own subspecies than to the other subspecies’ songs, whereas the second responded equally strongly to songs of both subspecies. While song parameters revealed a mixed pattern of divergence between allopatric and parapatric populations, the majority of spectral characteristics showed increased divergence in parapatry, suggestive of character displacement. This increased song divergence in parapatry appeared to affect behavioral responses to playback as discriminating responses were most prominent in parapatry and against parapatric songs. The clear behavioral impact of subspecies‐specific song differences supports a potential role for song as an acoustic barrier to gene flow. The asymmetric nature of the responses suggests that song divergence could affect the direction of gene flow and the position of the subspecies‐specific transition.

Risky Ripples Allow Bats and Frogs to Eavesdrop on a Multisensory Sexual Display

Animal displays are often perceived by intended and unintended receivers in more than one sensory system. In addition, cues that are an incidental consequence of signal production can also be perceived by different receivers, even when the receivers use different sensory systems to perceive them. Here we show that the vocal responses of male túngara frogs (Physalaemus pustulosus) increase twofold when call-induced water ripples are added to the acoustic component of a rival’s call. Hunting bats (Trachops cirrhosus) can echolocate this signal by-product and prefer to attack model frogs when ripples are added to the acoustic component of the call. This study illustrates how the perception of a signal by-product by intended and unintended receivers through different sensory systems generates both costs and benefits for the signaler. Calling frogs incidentally produce water ripples that are targeted by rival males and frog-eating bats. Its Complicated Animals have evolved impressive displays used in mate selection. Although intended for the opposite sex of the same species, the potential for eavesdropping is significant. In cases where the sensory signature is the sexual signal itself (such as a bird call), selection from harmful eavesdroppers could result in a reduction in signal intensity that represents a balance between the cost and benefit of the signal. Halfwerk et al. (p. 413), however, show that the physical by-product of a signal can also act as a cue to both intended and eavesdropping recipients. Ripples in the water made by throat sac expansion in calling túngara frogs signal their presence both to rivals and to predatory bats. This physical signature of the call itself cannot be modified; thus, it represents a cost-benefit ratio to calling that cannot be shifted through selection pressure from either side. Thus, physical by-products of sensory signaling create significant complexity in the evolution of sexual signaling.

Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance

Anthropogenic sensory pollution is affecting ecosystems worldwide. Human actions generate acoustic noise, emanate artificial light and emit chemical substances. All of these pollutants are known to affect animals. Most studies on anthropogenic pollution address the impact of pollutants in unimodal sensory domains. High levels of anthropogenic noise, for example, have been shown to interfere with acoustic signals and cues. However, animals rely on multiple senses, and pollutants often co-occur. Thus, a full ecological assessment of the impact of anthropogenic activities requires a multimodal approach. We describe how sensory pollutants can co-occur and how covariance among pollutants may differ from natural situations. We review how animals combine information that arrives at their sensory systems through different modalities and outline how sensory conditions can interfere with multimodal perception. Finally, we describe how sensory pollutants can affect the perception, behaviour and endocrinology of animals within and across sensory modalities. We conclude that sensory pollution can affect animals in complex ways due to interactions among sensory stimuli, neural processing and behavioural and endocrinal feedback. We call for more empirical data on covariance among sensory conditions, for instance, data on correlated levels in noise and light pollution. Furthermore, we encourage researchers to test animal responses to a full-factorial set of sensory pollutants in the presence or the absence of ecologically important signals and cues. We realize that such approach is often time and energy consuming, but we think this is the only way to fully understand the multimodal impact of sensory pollution on animal performance and perception.

Behavioural ecology: noise annoys at community level.

A new study on the impact of anthropogenic noise on birds takes a behavioural discipline to the level of community ecology: noise can not only harm individual species but also alter species relationships.

Birds and Anthropogenic Noise: Singing Higher May Matter

In a recent theoretical study, Nemeth and Brumm explored the effect of amplitude and frequency variation in birdsongs on signal transmission in forested and noisy urban environments. They argued that “increased song pitch might not be an adaptation” but “an epiphenomenon of urbanization.” Here we address the validity of comparing the communication benefits of changes in amplitude and frequency to question the adaptive significance of “urban songs.” We believe that their calculations actually confirm considerable high-frequency benefits under noisy urban conditions, between and within species. Hence, we conclude that noise-dependent frequency shifts in urban birds can be adaptive.

Bats perceptually weight prey cues across sensory systems when hunting in noise

Anthropogenic noise can interfere with environmental information processing and thereby reduce survival and reproduction. Receivers of signals and cues in particular depend on perceptual strategies to adjust to noisy conditions. We found that predators that hunt using prey sounds can reduce the negative impact of noise by making use of prey cues conveyed through additional sensory systems. In the presence of masking noise, but not in its absence, frog-eating bats preferred and were faster in attacking a robotic frog emitting multiple sensory cues. The behavioral changes induced by masking noise were accompanied by an increase in active localization through echolocation. Our findings help to reveal how animals can adapt to anthropogenic noise and have implications for the role of sensory ecology in driving species interactions.