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.

Singing strategies are linked to perch use on foraging territories in heart-nosed bats

Acoustic communication allows animals to coordinate and optimize resource utilization in space. Cardioderma cor, the heart-nosed bat, is one of the few species of bats known to sing during nighttime foraging. Previous research found that heart-nosed bats react aggressively to song playback, supporting the territorial defense hypothesis of singing in this species. By tracking 14 individuals nightly during the dry seasons in Tanzania we further investigated the territorial defense hypothesis from an ecological standpoint, which predicts singing should be associated with exclusive areas containing a resource. We quantified the singing behavior of individuals at all perches used throughout the night. Using home range analysis tools, we quantified overall use night ranges and singing ranges, as well as areas used in early and later time periods at night. Males engaged in antiphonal singing from small (x̄ = 3.48 ± 2.71 ha), largely exclusive areas that overlapped with overall night ranges used for gleaning prey. Individuals varied in singing effort; however, all sang significantly more as night progressed. Subsequently, areas used earlier at night and overall use areas were both larger than singing areas. Individuals varied in singing strategies. Some males sang for long periods in particular trees and had smaller core areas, while others moved frequently among singing trees. The most prolific singers used more perches overall. The results support the hypothesis that acoustic communication repertoires evolved in support of stable foraging territory advertisement and defense in some bats.

Learning in advance? Interspecific recognition ability in male Eurasian blackcaps

Interspecific aggression is common in bird communities. It is thought to be a consequence of learned behavior or misdirected intraspecific aggression. In the former case birds acquire the ability to identify individuals of other species by social learning of species-specific traits during interactions with heterospecifics in a shared habitat. I conducted a two-choice song playback experiment to investigate the role of associating signals from two sensory modalities, auditory and visual, in shaping the agonistic response of male Eurasian Blackcaps (Sylvia atricapilla) to simulated male Garden Warbler (S. borin) intruders. I measured focal males’ response to playbacks to the song of a Blackcap or a Garden Warbler while giving them a choice between stuffed male models of both species presented in their territories. The experiments were carried out in early spring, before the arrival of Garden Warblers from Africa. I found that male Blackcaps were able to associate species-specific songs with species-specific plumage types. The ability to associate signals characterized not only experienced after-second-year old males, but also second-year old males that had not had the opportunity to defend breeding territories against heterospecifics. This suggests that second-year old male Blackcaps acquire the ability to associate Garden Warbler song with plumage before they use this skill when defending territory during their first breeding episode. Male Blackcaps do not mistake male Garden Warblers for males of their species, but rather learn these associations during the first months of life. However, the possibility that these associations are innate cannot be excluded.

Vocal recognition suggests premating isolation between lineages of a lekking hummingbird

Species with genetically differentiated allopatric populations commonly differ in phenotypic traits due to drift and/or selection, which can be important drivers of reproductive isolation. Wedge-tailed sabrewing (Campylopterus curvipennis) is a species complex composed of three genetically and acoustically differentiated allopatric lineages that correspond to currently recognized subspecies in Mexico: C. c. curvipennis (Sierra Madre Oriental), C. c. pampa (Yucatán Peninsula), and C. c. excellens (Los Tuxtlas). Although excellens is taxonomically recognized as a distinct species, there is genetic evidence that lineages excellens and curvipennis have diverged from each other later than pampa. In this study, we experimentally tested C. c. curvipennis song recognition as a major factor in premating reproductive isolation for lineage recognition. To this end, we conducted a song playback experiment to test whether territorial males of one C. c. curvipennis lek discriminate among potential competitors based on male songs from the three lineages. Males of curvipennis responded more aggressively to songs of their own lineage and excellens, than to songs of the most divergent lineage pampa, as evidenced by significant differences in a variety of intensity and latency response variables. This indicate that the pampa male song does not represent a competitive threat as curvipennis and excellens songs, in which divergence and song recognition represent premating reproductive isolation between these isolated lineages. However, the acoustic limits between curvipennis and excellens might be attenuated by gene flow in case of secondary contact between them, despite the strong and relatively rapid divergence of their sexually selected song traits.

Tape lures swell bycatch on a Mediterranean island harbouring illegal bird trapping

Mediterranean islands are critical for migrating birds, providing shelter and sustenance for millions of individuals each year. Humans have long exploited bird migration through hunting and illegal trapping. On the island of Cyprus, trapping birds during their migratory peak is considered a local tradition, but has long been against the law. Illegal bird trapping is a lucrative business, however, with trappers using tape lures that broadcast species’ vocalizations because it is expected to increase numbers of target species. Yet, by how much the use of song playback increases capture rates remains underappreciated. In particular, it is not known whether song playback of target species affects bycatch rates. Here, we show with the use of playback experiments that song playback is highly effective in luring birds towards trapping sites. We found that playback increases six to eight times the number of individuals of target species captured, but also significantly increases bycatch. Our findings thus show that in contrast to popular belief that tape lures are a selective trapping method, they also lead to increased captures of non-target species, which can include species of conservation concern.

Multi-modal communication: song sparrows increase signal redundancy in noise

Although the effects of anthropogenic noise on animal communication have been studied widely, most research on the effect of noise in communication has focused on signals in a single modality. Consequently, how multi-modal communication is affected by anthropogenic noise is relatively poorly understood. Here, we ask whether song sparrows ( Melospiza melodia ) show evidence of plasticity in response to noise in two aggressive signals in acoustic and visual modalities. We test two hypotheses: (i) that song sparrows will shift signalling effort to the visual modality (the multi-modal shift hypothesis) and (ii) that they will increase redundancy of their multi-modal signalling (the back-up signal hypothesis). We presented male song sparrows with song playback and a taxidermic mount with or without a low-frequency acoustic noise from a nearby speaker. We found that males did not switch their signalling effort to visual modality (i.e. wing waves) in response to the noise. However, the correlation between warbled soft songs and wing waves increased in the noise treatment, i.e. signals became more redundant. These results suggest that when faced with anthropogenic noise, song sparrows can increase the redundancy of their multi-modal signals, which may aid in the robustness of the communication system.

Dopamine in the songbird auditory cortex shapes auditory preference

ABSTRACTIn vocal communication, vocal signals can provide listeners with information and also elicit motivated responses. Auditory cortical and mesolimbic reward circuits are often considered to have distinct roles in these processes, with auditory cortical circuits responsible for detecting and discriminating sounds and mesolimbic circuits ascribing salience and modulating preference for those sounds. Here, we investigated whether dopamine within auditory cortical circuits themselves can shape the incentive salience of a vocal signal. Using female zebra finches, who show natural preferences for vocal signals produced by males (‘songs’), we found that pairing passive song playback with pharmacological manipulations of dopamine in the secondary auditory cortex drives changes to song preferences. Plasticity of song preferences by dopamine lasted for at least one week and was not influenced by norepinephrine manipulations. These data suggest that dopamine acting directly in sensory processing areas can shape the incentive salience of communication signals.

Multi-modal communication: Song sparrows increase signal redundancy in noise

Although the effects of anthropogenic noise on animal communication have been studied widely, most research on the effect of noise in communication has been on communication in a single modality. Consequently, how multimodal communication is affected by anthropogenic noise is relatively poorly understood. Here we ask whether song sparrows (Melospiza melodia) show evidence of plasticity in response to noise in two aggressive signals in acoustic and visual modalities. We test two hypotheses: (1) that song sparrows will shift signaling effort to the visual modality (the multi-modal shift hypothesis), and (2) that they will increase redundancy of their multi-modal signaling (the back-up hypothesis). We presented male song sparrows with song playback and a taxidermic mount with or without a low-frequency acoustic noise from a nearby speaker. We found that males did not switch their signaling effort to visual modality (i.e., wing waves) in response to the noise. However, the correlation between warbled soft songs and wing waves increased in the noise treatment, i.e. signals became more redundant. These results suggest that when faced with anthropogenic noise, song sparrows can increase redundancy of their multi-modal signals, which may aid in robustness of the communication system.

Differential developmental changes in cortical representations of auditory-vocal stimuli in songbirds

Procedural skill learning requires iterative comparisons between feedback of self-generated motor output and a goal sensorimotor pattern. In juvenile songbirds, neural representations of both self-generated behaviors (each bird’s own immature song) and the goal motor pattern (each bird’s adult tutor song) are essential for vocal learning, yet little is known about how these behaviorally relevant stimuli are encoded. We made extracellular recordings during song playback in anesthetized juvenile and adult zebra finches ( Taeniopygia guttata) in adjacent cortical regions RA (robust nucleus of the arcopallium), AId (dorsal intermediate arcopallium), and RA cup, each of which is well situated to integrate auditory-vocal information: RA is a motor cortical region that drives vocal output, AId is an adjoining cortical region whose projections converge with basal ganglia loops for song learning in the dorsal thalamus, and RA cup surrounds RA and receives inputs from primary and secondary auditory cortex. We found strong developmental differences in neural selectivity within RA, but not in AId or RA cup. Juvenile RA neurons were broadly responsive to multiple songs but preferred juvenile over adult vocal sounds; in addition, spiking responses lacked consistent temporal patterning. By adulthood, RA neurons responded most strongly to each bird’s own song with precisely timed spiking activity. In contrast, we observed a complete lack of song responsivity in both juvenile and adult AId, even though this region receives song-responsive inputs. A surprisingly large proportion of sites in RA cup of both juveniles and adults did not respond to song playback, and responsive sites showed little evidence of song selectivity. NEW & NOTEWORTHY Motor skill learning entails changes in selectivity for behaviorally relevant stimuli across cortical regions, yet the neural representation of these stimuli remains understudied. We investigated how information important for vocal learning in zebra finches is represented in regions analogous to infragranular layers of motor and auditory cortices during vs. after the developmentally regulated learning period. The results provide insight into how neurons in higher level stages of cortical processing represent stimuli important for motor skill learning.

Subspecies status and methods explain strength of response to local versus foreign song by oscine birds in meta-analysis

To understand the implications of geographical variation in vocal culture in songbirds, researchers have often compared territorial responses to playback of local songs versus responses to playback of songs from ‘foreign’ conspecifics. This body of work has the potential to help us move towards a general understanding of factors driving divergence in signal recognition. We conducted a systematic review and meta-analysis of 57 playback studies to explain variation in strength of response to local versus foreign songs. Studies with incomplete reporting of results had elevated effects due to selective reporting. Studies that used small numbers of stimuli as exemplars (pseudoreplication) had more variable effects than studies without severe pseudoreplication. Whether or not we controlled for pseudoreplication, we found greater response to playback of local song than to foreign song. In investigating potential biological drivers of the variation in strength of experimental effects, we found that the difference in territorial response to local versus foreign song was stronger if the foreign song was recorded from another subspecies than if the foreign song was recorded from the same subspecies as the focal individuals. Indexes of risk of accidental response to heterospecific song did not coherently explain response to foreign conspecific songs, nor did factors expected to influence individual experience with foreign conspecific songs. Thus, although oscine songbirds clearly react more aggressively to local song than to foreign song and variation in the strength of this effect is influenced by methodological choices and subspecies status, considerable variation in the strength of response to local versus foreign song playback remains to be explained.