Animal cognition: Wild mountain chickadees follow the abstract rules.

concept formation is a cognitive skill that nonhuman animals have been shown to possess. Most often, this ability has been shown in laboratory tasks; a new study sheds light on what role abstract concept formation may play in the wild.

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.

Effect of feed-time duration on discrimination of vocalizations in a go/no-go operant paradigm.

Refining and modifying experimental procedures play a vital role in improving methodology while also reducing animal distress. In this study, we asked if an increase in feed time duration affects discrimination in an operant go/no-go task. Specifically, we used zebra finches' sexually dimorphic distance calls as acoustic stimuli to test whether there were any significant differences in performance on an operant discrimination task requiring zebra finches to classify calls according to the sex of the producer when a key experimental parameter, feed time duration, was increased from 1 s to 2 s. We found no differences in learning speed (trials to criterion) between birds that were given 1 s or 2 s of food access following a correct go response. Our results indicate doubling food access duration did not impact the speed of acquisition of distance call discrimination in zebra finches. These findings suggest that we can provide twice as much time for zebra finches to access food, potentially improving animal welfare, with no impact on experimental outcomes.

Comparing methodologies for classification of zebra finch distance calls.

Bioacoustic analysis has been used for a variety of purposes including classifying vocalizations for biodiversity monitoring and understanding mechanisms of cognitive processes. A wide range of statistical methods, including various automated methods, have been used to successfully classify vocalizations based on species, sex, geography, and individual. A comprehensive approach focusing on identifying acoustic features putatively involved in classification is required for the prediction of features necessary for discrimination in the real world. Here, we used several classification techniques, namely discriminant function analyses (DFAs), support vector machines (SVMs), and artificial neural networks (ANNs), for sex-based classification of zebra finch (Taeniopygia guttata) distance calls using acoustic features measured from spectrograms. We found that all three methods (DFAs, SVMs, and ANNs) correctly classified the calls to respective sex-based categories with high accuracy between 92 and 96%. Frequency modulation of ascending frequency, total duration, and end frequency of the distance call were the most predictive features underlying this classification in all of our models. Our results corroborate evidence of the importance of total call duration and frequency modulation in the classification of male and female distance calls. Moreover, we provide a methodological approach for bioacoustic classification problems using multiple statistical analyses.

Pitch chroma information is processed in addition to pitch height information with more than two pitch-range categories.

Octave equivalence describes the perception that notes separated by a doubling in frequency sound similar. While the octave is used cross-culturally as a basis of pitch perception, experimental demonstration of the phenomenon has proved to be difficult. In past work, members of our group developed a three-range generalization paradigm that reliably demonstrated octave equivalence. In this study we replicate and expand on this previous work trying to answer three questions that help us understand the origins and potential cross-cultural significance of octave equivalence: (1) whether training with three ranges is strictly necessary or whether an easier-to-learn two-range task would be sufficient, (2) whether the task could demonstrate octave equivalence beyond neighbouring octaves, and (3) whether language skills and musical education impact the use of octave equivalence in this task. We conducted a large-sample study using variations of the original paradigm to answer these questions. Results found here suggest that the three-range discrimination task is indeed vital to demonstrating octave equivalence. In a two-range task, pitch height appears to be dominant over octave equivalence. Octave equivalence has an effect only when pitch height alone is not sufficient. Results also suggest that effects of octave equivalence are strongest between neighbouring octaves, and that tonal language and musical training have a positive effect on learning of discriminations but not on perception of octave equivalence during testing. We discuss these results considering their relevance to future research and to ongoing debates about the basis of octave equivalence perception.

Among-individual differences in auditory and physical cognitive abilities in zebra finches.

Among-individual variation in performance on cognitive tasks is ubiquitous across species that have been examined, and understanding the evolution of cognitive abilities requires investigating among-individual variation because natural selection acts on individual differences. However, relatively little is known about the extent to which individual differences in cognition are determined by domain-specific compared with domain-general cognitive abilities. We examined individual differences in learning speed of zebra finches across seven different tasks to determine the extent of domain-specific versus domain-general learning abilities, as well as the relationship between learning speed and learning generalization. Thirty-two zebra finches completed a foraging board experiment that included visual and structural discriminations, and then these same birds went through an acoustic operant discrimination experiment that required discriminating between different natural categories of acoustic stimuli. We found evidence of domain-general learning abilities as birds' relative performance on the seven learning tasks was weakly repeatable and a principal components analysis found a first principal component that explained 36% of the variance in performance across tasks with all tasks loading unidirectionally on this component. However, the few significant correlations between tasks and high repeatability within each experiment suggest the potential for domain-specific abilities. Learning speed did not influence an individual's ability to generalize learning. These results suggest that zebra finch performance across visual, structural, and auditory learning relies upon some common mechanism; some might call this evidence of "general intelligence"(g), but it is also possible that this finding is due to other noncognitive mechanisms such as motivation.

Individual acoustic differences in female black-capped chickadee (poecile atricapillus) fee-bee songs.

In songbirds, song has traditionally been considered a vocalization mainly produced by males. However, recent research suggests that both sexes produce song. While the function and structure of male black-capped chickadee (Poecile atricapillus) fee-bee song have been well-studied, research on female song is comparatively limited. Past discrimination and playback studies have shown that male black-capped chickadees can discriminate between individual males via their fee-bee songs. Recently, we have shown that male and female black-capped chickadees can identify individual females via their fee-bee song even when presented with only the bee position of the song. Our results using discriminant function analyses (DFA) support that female songs are individually distinctive. We found that songs could be correctly classified to the individual (81%) and season (97%) based on several acoustic features including but not limited to bee-note duration and fee-note peak frequency. In addition, an artificial neural network was trained to identify individuals based on the selected DFA acoustic features and was able to achieve 90% accuracy by individual and 93% by season. While this study provides a quantitative description of the acoustic structure of female song, the perception and function of female song in this species requires further investigation.

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.

Unifying psychological and biological approaches to understanding animal cognition.

This special issue has two main aims. The first aim is to broaden the scope of the Canadian Journal of Experimental Psychology. This aim is motivated by the simple fact that the journal's mandate includes comparative psychology, but many of the articles published in the journal are currently, and have been for some time, mainly human cognitive in nature. The second aim of this issue is one that we take very seriously, and that is to promote not only comparative cognition and cognitive ecology research but research from a diverse group of scientists. Although the global diversity in this special issue is not exhaustive, there is work highlighted from scientists at institutions in Canada, Germany, Italy, the Netherlands, Spain, the United Kingdom, and the United States. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

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).

Sometimes a stick might just be a stick.

Suzuki (Proceedings of the Natural Academy of Sciences, 115, 1541-1545, 2018) conducted elegant field experiments examining referential communication in Japanese tits. Bond (Learning & Behavior, in press, 2019) explains some key considerations and future experimentation that should be conducted to solidify these conclusions. An important takeaway from both Suzuki and Bond is that scientists can, and should, both be excited for new, interesting scientific discoveries, and also view such findings with a critical, but collegial, eye for more parsimonious explanations and the manipulations required to test such explanations.

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.

How Much of Language Acquisition Does Operant Conditioning Explain?

Since the 1950s, when Chomsky argued that Skinner's arguments could not explain syntactic acquisition, psychologists have generally avoided explicitly invoking operant or instrumental conditioning as a learning mechanism for language among human children. In this article, we argue that this is a mistake. We focus on research that has been done on language learning in human infants and toddlers in order to illustrate our points. Researchers have ended up inventing learning mechanisms that, in actual practice, not only resemble but also in fact are examples of operant conditioning (OC) by any other name they select. We argue that language acquisition researchers should proceed by first ruling out OC before invoking alternative learning mechanisms. While it is possible that OC cannot explain all of the language acquisition, simple learning mechanisms that work across species may have some explanatory power in children's language learning.

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

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.

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.