ZENK expression in the auditory pathway of black-capped chickadees (Poecile atricapillus) as a function of D note number and duty cycle of chick-a-dee calls

Black-capped chickadees (Poecile atricapillus) use their namesake chick-a-dee call for multiple functions, altering the features of the call depending on context. For example, duty cycle (the proportion of time filled by vocalizations) and fine structure traits (e.g., number of D notes) can encode contextual factors, such as predator size and food quality. Wilson and Mennill (2011) found that chickadees show stronger behavioral responses to playback of chick-a-dee calls with higher duty cycles, but not to the number of D notes. That is, independent of the number of D notes in a call, but dependent on the overall proportion of time filled with vocalization, birds responded more to higher duty cycle playback compared to lower duty cycle playback. Here we presented chickadees with chick-a-dee calls that contained either two D (referred to hereafter as 2 D) notes with a low duty cycle, 2 D notes with a high duty cycle, 10 D notes with a high duty cycle, or 2 D notes with a high duty cycle but played in reverse (a non-signaling control). We then measured ZENK expression in the auditory nuclei where perceptual discrimination is thought to occur. Based on the behavioral results of Wilson and Mennill, 2011, we predicted we would observe the highest ZENK expression in response to forward-playing calls with high duty cycles; we predicted we would observe no significant difference in ZENK expression between forward-playing high duty cycle playbacks (2 D or 10 D). We found no significant difference between forward-playing 2 D and 10 D high duty cycle playbacks. However, contrary to our predictions, we did not find any effects of altering the duty cycle or note number presented

Black-capped Chickadee (Poecile atricapillus)

Recordings were provided by Marc Avey, Ph.D, Jenna V. Congdon, John Hoang, and Prof. Christopher B. Sturdy, Ph.D - Department of Psychology University of Alberta (Canada). Arousal was assessed based on research showing increase of neural activity in response to high-threat predator models: Avey, M. T., Hoeschele, M., Moscicki, M. K., Bloomfield, L. L., & Sturdy, C. B. (2011). Neural correlates of threat perception: neural equivalence of conspecific and heterospecific mobbing calls is learned. PLoS One, 6(8), e23844

Chickadee behavioural response to varying threat levels of predator and conspecific calls

Chickadees produce many vocalizations, including chick-a-dee calls which they use as a mobbing call in the presence of predators. Previous research has shown that chickadees produce more D notes in their mobbing calls in response to high-threat predators compared to low-threat predators, and may perceive predator and corresponding mobbing vocalizations as similar. We presented black-capped chickadees with playback of high- and low-threat predator calls and conspecific mobbing calls, and non-threat heterospecific and reversed mobbing calls, to examine vocal and movement behavioural responses. Chickadees produced more chick-a-dee calls in response to playback of calls produced by a high-threat predator compared to calls produced by a low-threat predator, and to reversed high-threat mobbing calls compared to normal (i.e., non-reversed) high-threat mobbing calls. Chickadees also vocalized more in response to all playback conditions consisting of conspecific mobbing calls compared to a silent baseline period. The number of D notes that the subjects produced was similar to previous findings; chickadees produced approximately one to three D notes per call in response to low-threat mobbing calls, and produced more calls containing four to five D notes in response to high-threat mobbing calls, although this difference in the number of D notes per call was not significant. The difference in chickadees’ production of tseet calls across playback conditions approached significance as chickadees called more in response to conspecific mobbing calls, but not in response to heterospecific calls. General movement activity decreased in response to playback of conspecific-produced vocalizations, but increased in response to heterospecific-produced vocalizations, suggesting that chickadees may mobilize more in response to predator playback in preparation for a “fight or flight” situation. These results also suggest that chickadees may produce more mobbing calls in response to high-threat predator vocalizations as an attempt to initiate mobbing with conspecifics, while they produce fewer mobbing calls in response to a low-threat predator that a chickadee could outmaneuver

Chickadee behavioural response to varying threat levels of predator and conspecific calls

Chickadees produce many vocalizations, including chick-a-dee calls which they use as a mobbing call in the presence of predators. Previous research has shown that chickadees produce more D notes in their mobbing calls in response to high-threat predators compared to low-threat predators, and may perceive predator and corresponding mobbing vocalizations as similar. We presented black-capped chickadees with playback of high- and low-threat predator calls and conspecific mobbing calls, and non-threat heterospecific and reversed mobbing calls, to examine vocal and movement behavioural responses. Chickadees produced more chick-a-dee calls in response to playback of calls produced by a high-threat predator compared to calls produced by a low-threat predator, and to reversed high-threat mobbing calls compared to normal (i.e., non-reversed) high-threat mobbing calls. Chickadees also vocalized more in response to all playback conditions consisting of conspecific mobbing calls compared to a silent baseline period. The number of D notes that the subjects produced was similar to previous findings; chickadees produced approximately one to three D notes per call in response to low-threat mobbing calls, and produced more calls containing four to five D notes in response to high-threat mobbing calls, although this difference in the number of D notes per call was not significant. The difference in chickadees’ production of tseet calls across playback conditions approached significance as chickadees called more in response to conspecific mobbing calls, but not in response to heterospecific calls. General movement activity decreased in response to playback of conspecific-produced vocalizations, but increased in response to heterospecific-produced vocalizations, suggesting that chickadees may mobilize more in response to predator playback in preparation for a “fight or flight” situation. These results also suggest that chickadees may produce more mobbing calls in response to high-threat predator vocalizations as an attempt to initiate mobbing with conspecifics, while they produce fewer mobbing calls in response to a low-threat predator that a chickadee could outmaneuver

Hear them roar: A comparison of black-capped chickadee (Poecile atricapillus) and human (Homo sapiens) perception of arousal in vocalizations across all classes of terrestrial vertebrates

Recently, evidence for acoustic universals in vocal communication was found by demonstrating that humans can identify levels of arousal in vocalizations produced by species across three biological classes (Filippi et al., 2017). Here, we extend this work by testing whether two vocal learning species, humans and chickadees, can discriminate vocalizations of high and low arousal using operant discrimination go/no-go tasks. Stimuli included vocalizations from nine species: giant panda, American alligator, common raven, hourglass treefrog, African elephant, Barbary macaque, domestic pig, black-capped chickadee, and human. Subjects were trained to respond to high or low arousal vocalizations, then tested with additional high and low arousal vocalizations produced by each species. Chickadees (Experiment 1) and humans (Experiment 2) learned to discriminate between high and low arousal stimuli and significantly transferred the discrimination to additional panda, human, and chickadee vocalizations. Finally, we conducted discriminant function analyses using four acoustic measures, finding evidence suggesting that fundamental frequency played a role in responding during the task. However, these analyses also suggest roles for other acoustic factors as well as familiarity. In sum, the results from these studies provide evidence that chickadees and humans are capable of perceiving arousal in vocalizations produced by multiple species

Humans recognize emotional arousal in vocalizations across all classes of terrestrial vertebrates: evidence for acoustic universals

International audienceWriting over a century ago, Darwin hypothesized that vocal expression of emotion dates back to our earliest terrestrial ancestors. If this hypothesis is true, we should expect to find cross-species acoustic universals in emotional vocalizations. Studies suggest that acoustic attributes of aroused vocalizations are shared across many mammalian species, and that humans can use these attributes to infer emotional content. But do these acoustic attributes extend to non-mammalian vertebrates? In this study, we asked human participants to judge the emotional content of vocalizations of nine vertebrate species representing three different biological classes—Amphibia, Reptilia (non-aves and aves) and Mammalia. We found that humans are able to identify higher levels of arousal in vocalizations across all species. This result was consistent across different language groups (English, German and Mandarin native speakers), suggesting that this ability is biologically rooted in humans. Our findings indicate that humans use multiple acoustic parameters to infer relative arousal in vocalizations for each species, but mainly rely on fundamental frequency and spectral centre of gravity to identify higher arousal vocalizations across species. These results suggest that fundamental mechanisms of vocal emotional expression are shared among vertebrates and could represent a homologous signalling system

The public interest

Writing over a century ago, Darwin hypothesized that vocal expression of emotion dates back to our earliest terrestrial ancestors. If this hypothesis is true, we should expect to find cross-species acoustic universals in emotional vocalizations. Studies suggest that acoustic attributes of aroused vocalizations are shared across many mammalian species, and that humans can use these attributes to infer emotional content. But do these acoustic attributes extend to non-mammalian vertebrates? In this study, we asked human participants to judge the emotional content of vocalizations of nine vertebrate species representing three different biological classes—Amphibia, Reptilia (non-aves and aves) and Mammalia. We found that humans are able to identify higher levels of arousal in vocalizations across all species. This result was consistent across different language groups (English, German and Mandarin native speakers), suggesting that this ability is biologically rooted in humans. Our findings indicate that humans use multiple acoustic parameters to infer relative arousal in vocalizations for each species, but mainly rely on fundamental frequency and spectral centre of gravity to identify higher arousal vocalizations across species. These results suggest that fundamental mechanisms of vocal emotional expression are shared among vertebrates and could represent a homologous signalling system

Black-capped chickadees categorize songs based on features that vary geographically

The songs of many songbird species vary geographically, yet, the songs of black-capped chickadees, Poecile atricapillus, show remarkable consistency across most of the species\u27 North American range. Previous research has described subtle variations in the song of this species by comparing songs produced by males at distant parts of the species\u27 range (British Columbia and Ontario). In the current study, we used an operant discrimination task to examine whether birds classify the songs produced by males in these two previously studied locations as belonging to distinct open-ended categories. In both experiments, when birds were presented with new songs, they continued to respond to songs from the same geographical location as the songs that were reinforced during initial discrimination training, suggesting that birds were using open-ended categorization. We also presented birds with songs in which we manipulated acoustic features in order to examine the acoustic mechanisms used during discrimination; results provide support that birds use the duration of the song when discriminating, but the results also suggest that birds used additional acoustic features. Taken together, these experiments show that black-capped chickadees classify songs into open-ended, geography-based categories, and provide compelling evidence that perceptible acoustic differences exist in a vocalization that is seemingly consistent across the species\u27 range. © 2015 The Association for the Study of Animal Behaviour