Black-capped chickadees (Poecile atricapillus) discriminate between naturally-ordered and scramble-ordered chick-a-dee calls and individual preference is related to rate of learning.

Though many forms of animal communication are not reliant on the order in which components of signals are combined to be effective, there is evidence that order does matter for some communication systems. In the light of differential responding to calls of varying note-order observed in black-capped chickadees in the field, we set out to determine whether chickadees recognize syntactically-ordered and incorrectly-ordered chick-a-dee calls as separate and distinct conceptual categories using both an auditory preference task and go/no-go operant conditioning paradigm. Results show that chickadees spent more time on the perch that did not produce sound (i.e., silent perch) than on either of the acoustic perches (i.e., natural and scrambled order chick-a-dee call playback) and visited the perch associated with naturally-ordered calls more often than the perch associated with scrambled-order calls. Birds in both the True natural- and scrambled-order call groups continued to respond according to the contingencies that they learned in Discrimination training, indicating that black-capped chickadees are capable of perceiving and acting upon the categories of natural- versus scrambled-ordered calls.

The impact of anthropogenic noise on individual identification via female song in Black-capped chickadees (Poecile atricapillus).

When anthropogenic noise occurs simultaneously with an acoustic signal or cue, it can be difficult for an animal to interpret the information encoded within vocalizations. However, limited research has focused on how anthropogenic noise affects the identification of acoustic communication signals. In songbirds, research has also shown that black-capped chickadees (Poecile atricapillus) will shift the pitch and change the frequency at which they sing in the presence of anthropogenic, and experimental noise. Black-capped chickadees produce several vocalizations; their fee-bee song is used for mate attraction and territorial defence, and contains information about dominance hierarchy and native geographic location. Previously, we demonstrated that black-capped chickadees can discriminate between individual female chickadees via their fee-bee songs. Here we used an operant discrimination go/no-go paradigm to discern whether the ability to discriminate between individual female chickadees by their song would be impacted by differing levels of anthropogenic noise. Following discrimination training, two levels of anthropogenic noise (low: 40 dB SPL; high: 75 dB SPL) were played with stimuli to determine how anthropogenic noise would impact discrimination. Results showed that even with low-level noise (40 dB SPL) performance decreased and high-level (75 dB SPL) noise was increasingly detrimental to discrimination. We learned that perception of fee-bee songs does change in the presence of anthropogenic noise such that birds take significantly longer to learn to discriminate between females, but birds were able to generalize responding after learning the discrimination. These results add to the growing literature underscoring the impact of human-made noise on avian wildlife, specifically the impact on perception of auditory signals.

Can you hear me now? The effect of signal degradation on perceived predator threat in black-capped chickadees (Poecile atricapillus).

Avian predators vary in their degree-of-threat to chickadees; for example, smaller owls and hawks are of higher threat to chickadees as they can easily maneuver through the trees, while larger predators cannot. We conducted an operant go/no-go discrimination task to investigate the effect of signal degradation on perceived threat. Chickadees were trained to respond to high-threat northern saw-whet owl (NSWO) or low-threat great horned owl (GHOW) calls that were recorded at short distances, and then tested with high- and low-threat owl calls that were rebroadcast and re-recorded across six distances (25 m, 50 m, 75 m, 100 m, 150 m, and 200 m). Subjects were further tested with high-threat and low-threat synthetic tones produced to mimic the natural calls across the six distances. We predicted that birds would perceive and respond to: (1) high-threat predator calls at longer distances compared to low-threat predator calls, and (2) synthetic tones similarly compared to the stimuli that they were designed to mimic. We believed chickadees would continue to perceive and respond to predators that pose a high threat at further distances; however, only responding to low-threat stimuli was consistent across distance recordings. Synthetic tones were treated similarly to natural stimuli but at lower response levels. Thus, the results of this study provide insights into how chickadees perceive threat.

Acoustic discrimination of predators by black-capped chickadees (Poecile atricapillus).

Smaller owls and hawks are high-threat predators to small songbirds, like chickadees, in comparison to larger avian predators due to smaller raptors' agility (Templeton et al. in Proc Natl Acad Sci 104:5479-5482, 2005). The current literature focuses only on high- and low-threat predators. We propose that there may be a continuum in threat perception. In the current study, we conducted an operant go/no-go experiment investigating black-capped chickadees' acoustic discrimination of predator threat. After obtaining eight hawk and eight owl species' calls, we assigned each species as: (1) large, low-threat, (2) mid-sized, unknown-threat and (3) small-, high-threat predators, according to wingspan and body size. Black-capped chickadees were either trained to respond ('go') to high-threat predator calls or respond to low-threat predator calls. When either low-threat predator calls were not reinforced or high-threat predator calls were not reinforced the birds were to withhold responding ('no-go') to those stimuli. We then tested transfer of training with additional small and large predator calls, as well as with the calls of several mid-sized predators. We confirmed that chickadees can discriminate between high- and low-threat predator calls. We further investigated how chickadees categorize mid-sized species' calls by assessing transfer of training to previously non-differentially reinforced (i.e., pretraining) calls. Specifically, transfer test results suggest that mid-sized broad-winged hawks were perceived to be of high threat whereas mid-sized short-eared owls were perceived to be of low threat. However, mid-sized Cooper's hawks and northern hawk owls were not significantly differentially responded to, suggesting that they are of medium threat which supports the notion that perception of threat is along a continuum rather than distinct categories of high or low threat.

Abcam Monoclonal Egr-1 ab133695 is an effective primary antibody replacement for Santa Cruz sc-189 polyclonal Egr-1 in songbirds.

BACKGROUND: The immediate early gene ZENK (acronym zif268, Egr-1, NGFI-A, krox24) has been used extensively in songbird research (Mello et al., 1992; Jarvis and Nottebohm, 1997), as well as other research areas. ZENK has been used in assessing learning and memory, measuring neural activation, and identifying the cellular and molecular substrates involved in the first stages of memory formation (Watson and Clements, 1980). Previous songbird research has found that neurons located within the areas involved in auditory perception, namely the caudomedial nidopallium and caudomedial mesopallium, exhibit high levels of ZENK protein expression in response to conspecific songs and calls (Mello and Ribeiro, 1998; Avey et al., 2011). NEW METHOD: In large part due to its neuronal-specific labeling of ZENK protein, Santa Cruz Egr-1 sc-189 has been widely accepted as the standard primary antibody in songbird research. However, Santa Cruz Biotechnology Egr-1 no longer specifically labels and has also discontinued production of Egr-1 sc-189. Thus, the current study is focused on analyzing the effectiveness of alternative primary antibodies: Abcam polyclonal c-Fos, Abcam monoclonal ab133695 Egr-1, and Proteintech polyclonal Egr-1. RESULTS: Abcam monoclonal Egr-1 was successful in specifically labeling ZENK positive cells in the songbird auditory nuclei. Abcam polyclonal c-Fos and Proteintech polyclonal Egr-1 were found to have non-specific labeling. COMPARISON WITH EXISTING METHODS: Abcam monoclonal Egr-1 ab133695 was found to produce differential and specific labeling in the targeted auditory nuclei similar to previous studies successfully using Santa Cruz polyclonal Egr-1 (i.e. Mello and Ribeiro, 1998). CONCLUSIONS: Abcam monoclonal Egr-1 effectively labels ZENK in the songbird auditory nuclei, making it a suitable primary antibody replacement for Santa Cruz polyclonal Egr-1.

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. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

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.

The effects of anthropogenic noise on feeding behaviour in black-capped chickadees (Poecile atricapillus).

Anthropogenic noise has been shown to impact animal behaviour. Most studies investigating anthropogenic noise, and the detrimental effect it has on behaviour, have been conducted in the field, where a myriad of covariates can make interpretation challenging. In this experiment, we studied the effects of an approximation of anthropogenic noise, simulated with brown noise, on the feeding behaviour of wild-caught black-capped chickadees in a laboratory setting. We measured the amount of time spent eating while subjects heard either conspecific calls, brown noise, or a combination of calls and brown noise. We found that subjects fed more in the silence following playback than during the playback itself for all types of stimuli, suggesting that chickadees may shift their feeding behaviour to avoid feeding during periods of noise. The ability to adapt to changing environments (e.g., varying noise levels) may allow species to thrive in the presence of anthropogenic noise. Our findings outline a laboratory-based method that could be adopted and adapted to examine a variety avian species and of types anthropogenic noise.

ZENK expression following conspecific and heterospecific playback in the zebra finch auditory forebrain.

Zebra finches (Taeniopygia guttata) are sexually dimorphic songbirds, not only in appearance but also in vocal production: while males produce both calls and songs, females only produce calls. This dimorphism provides a means to contrast the auditory perception of vocalizations produced by songbird species of varying degrees of relatedness in a dimorphic species to that of a monomorphic species, species in which both males and females produce calls and songs (e.g., black-capped chickadees, Poecile atricapillus). In the current study, we examined neuronal expression after playback of acoustically similar hetero- and conspecific calls produced by species of differing phylogenetic relatedness to our subject species, zebra finch. We measured the immediate early gene (IEG) ZENK in two auditory areas of the forebrain (caudomedial mesopallium, CMM, and caudomedial nidopallium, NCM). We found no significant differences in ZENK expression in either male or female zebra finches regardless of playback condition. We also discuss comparisons between our results and the results of a previous study conducted by Avey et al. [1] on black-capped chickadees that used similar stimulus types. These results are consistent with the previous study which also found no significant differences in expression following playback of calls produced by various heterospecific species and conspecifics [1]. Our results suggest that, similar to black-capped chickadees, IEG expression in zebra finch CMM and NCM is tied to the acoustic similarity of vocalizations and not the phylogenetic relatedness of the species producing the vocalizations.

Chickadees discriminate contingency reversals presented consistently, but not frequently.

Chickadees are high-metabolism, non-migratory birds, and thus an especially interesting model for studying how animals follow patterns of food availability over time. Here, we studied whether black-capped chickadees (Poecile atricapillus) could learn to reverse their behavior and/or to anticipate changes in reinforcement when the reinforcer contingencies for each stimulus were not stably fixed in time. In Experiment 1, we examined the responses of chickadees on an auditory go/no-go task, with constant reversals in reinforcement contingencies every 120 trials across daily testing intervals. Chickadees did not produce above-chance discrimination; however, when trained with a procedure that only reversed after successful discrimination, chickadees were able to discriminate and reverse their behavior successfully. In Experiment 2, we examined the responses of chickadees when reversals were structured to occur at the same time once per day, and chickadees were again able to discriminate and reverse their behavior over time, though they showed no reliable evidence of reversal anticipation. The frequency of reversals throughout the day thus appears to be an important determinant for these animals' performance in reversal procedures.

Discrimination of acoustically similar conspecific and heterospecific vocalizations by black-capped chickadees (Poecile atricapillus).

Chickadees produce a multi-note chick-a-dee call in multiple socially relevant contexts. One component of this call is the D note, which is a low-frequency and acoustically complex note with a harmonic-like structure. In the current study, we tested black-capped chickadees on a between-category operant discrimination task using vocalizations with acoustic structures similar to black-capped chickadee D notes, but produced by various songbird species, in order to examine the role that phylogenetic distance plays in acoustic perception of vocal signals. We assessed the extent to which discrimination performance was influenced by the phylogenetic relatedness among the species producing the vocalizations and by the phylogenetic relatedness between the subjects' species (black-capped chickadees) and the vocalizers' species. We also conducted a bioacoustic analysis and discriminant function analysis in order to examine the acoustic similarities among the discrimination stimuli. A previous study has shown that neural activation in black-capped chickadee auditory and perceptual brain regions is similar following the presentation of these vocalization categories. However, we found that chickadees had difficulty discriminating between forward and reversed black-capped chickadee D notes, a result that directly corresponded to the bioacoustic analysis indicating that these stimulus categories were acoustically similar. In addition, our results suggest that the discrimination between vocalizations produced by two parid species (chestnut-backed chickadees and tufted titmice) is perceptually difficult for black-capped chickadees, a finding that is likely in part because these vocalizations contain acoustic similarities. Overall, our results provide evidence that black-capped chickadees' perceptual abilities are influenced by both phylogenetic relatedness and acoustic structure.

Bilateral lesions of nucleus subpretectalis/interstitio-pretecto-subpretectalis (SP/IPS) selectively impair figure-ground discrimination in pigeons.

Earlier, we reported that nucleus rotundus (Rt) together with its inhibitory complex, nucleus subpretectalis/interstitio-pretecto-subpretectalis (SP/IPS), had significantly higher activity in pigeons performing figure-ground discrimination than in the control group that did not perform any visual discriminations. In contrast, color discrimination produced significantly higher activity than control in the Rt but not in the SP/IPS. Finally, shape discrimination produced significantly lower activity than control in both the Rt and the SP/IPS. In this study, we trained pigeons to simultaneously perform three visual discriminations (figure-ground, color, and shape) using the same stimulus displays. When birds learned to perform all three tasks concurrently at high levels of accuracy, we conducted bilateral chemical lesions of the SP/IPS. After a period of recovery, the birds were retrained on the same tasks to evaluate the effect of lesions on maintenance of these discriminations. We found that the lesions of the SP/IPS had no effect on color or shape discrimination and that they significantly impaired figure-ground discrimination. Together with our earlier data, these results suggest that the nucleus Rt and the SP/IPS are the key structures involved in figure-ground discrimination. These results also imply that thalamic processing is critical for figure-ground segregation in avian brain.