Marisa Hoeschele

Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task

Animal personality, defined as consistent individual differences across context and time, has attracted much recent research interest in the study of animal behaviour. More recently, this field has begun to examine how such variation arose and is maintained within populations. The habitat-dependent selection hypothesis, which posits that animals with differing personality types may fare better (i.e. have a fitness advantage) in different habitats, suggests one possible mechanism. In the current experiment, we tested whether slow- and fast-exploring black-capped chickadees (Poecile atricapillus), determined by performance in a novel environment exploration task, perform differentially when the demands of an acoustic operant discrimination (cognitive) task were altered following successful task acquisition. We found that slow-exploring birds learn to reverse previously learned natural category rules more quickly than faster exploring conspecifics. In accordance with the habitat-dependent selection hypothesis, and previous work with great tits (Parus major), a close relative of the black-capped chickadee, our results suggest that fast-exploring birds may perform better in stable, predictable environments where forming a routine is advantageous, while slow-exploring birds are favoured in unstable, unpredictable environments, where task demands often change. Our results also support a hypothesis derived from previous work with great tits; slow-exploring birds may be generally more flexible (i.e. able to modify their behaviour in accordance with changes in environmental stimuli) in some learning tasks.

Individual differences in learning speed, performance accuracy and exploratory behaviour in black-capped chickadees

Cognitive processes are important to animals because they not only influence how animals acquire, store and recall information, but also may underpin behaviours such as deciding where to look for food, build a nest, or with whom to mate. Several recent studies have begun to examine the potential interaction between variation in cognition and variation in personality traits. One hypothesis proposed that there is a speed–accuracy trade-off in cognition ability that aligns with a fast–slow behaviour type. Here, we explicitly examined this hypothesis by testing wild-caught black-capped chickadees in a series of cognitive tasks that assessed both learning speed (the number of trials taken to learn) and accuracy (post-acquisition performance when tested with un-trained exemplars). Chickadees’ exploration scores were measured in a novel environment task. We found that slow-exploring chickadees demonstrated higher accuracy during the test phase, but did not learn the initial task in fewer trials compared to fast-exploring chickadees, providing partial support for the proposed link between cognition and personality. We report positive correlations in learning speed between different phases within cognitive tasks, but not between the three cognitive tasks suggesting independence in underlying cognitive processing. We discuss different rule-based strategies that may contribute to differential performance accuracy in cognitive tasks and provide suggestions for future experimentation to examine mechanisms underlying the relationship between cognition and personality.

Dominance signalled in an acoustic ornament

In many species, males use auditory signals to attract females and females select males based on their dominance status. Here we show that information on dominance status in male black-capped chickadees, Poecile atricapillus, a small, temperate, North American songbird, can be extracted from individual songs. We found that the relative amplitude of the two notes in the ‘fee bee’ song of this species was more consistent in dominant males. Furthermore, females responded differently to presentations of single song exemplars from males of different dominance status, with females vocalizing more and performing more motor behaviours during the presentation of dominant songs. Our study suggests that non-pitch-based cues within single vocalizations can both reliably indicate relative rank and be discriminated by females. 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. The concept of dominance was first developed by SchjelderupEbbe (1935) when studying fowl (Gallus gallus), who coined the term ‘pecking order’. Today, dominance has taken on broader meanings. Dominance is a relative measure based on encounters between individuals in which one individual asserts itself over another. Such hierarchies among individuals that repeatedly interact with one another serve to reduce future aggressive interactions. How individual animals display their dominance status to conspecifics is a matter of great importance for intra- and intersexual communication. In particular, being a dominant male

Neural Correlates of Threat Perception: Neural Equivalence of Conspecific and Heterospecific Mobbing Calls Is Learned

Songbird auditory areas (i.e., CMM and NCM) are preferentially activated to playback of conspecific vocalizations relative to heterospecific and arbitrary noise [1]–[2]. Here, we asked if the neural response to auditory stimulation is not simply preferential for conspecific vocalizations but also for the information conveyed by the vocalization. Black-capped chickadees use their chick-a-dee mobbing call to recruit conspecifics and other avian species to mob perched predators [3]. Mobbing calls produced in response to smaller, higher-threat predators contain more “D” notes compared to those produced in response to larger, lower-threat predators and thus convey the degree of threat of predators [4]. We specifically asked whether the neural response varies with the degree of threat conveyed by the mobbing calls of chickadees and whether the neural response is the same for actual predator calls that correspond to the degree of threat of the chickadee mobbing calls. Our results demonstrate that, as degree of threat increases in conspecific chickadee mobbing calls, there is a corresponding increase in immediate early gene (IEG) expression in telencephalic auditory areas. We also demonstrate that as the degree of threat increases for the heterospecific predator, there is a corresponding increase in IEG expression in the auditory areas. Furthermore, there was no significant difference in the amount IEG expression between conspecific mobbing calls or heterospecific predator calls that were the same degree of threat. In a second experiment, using hand-reared chickadees without predator experience, we found more IEG expression in response to mobbing calls than corresponding predator calls, indicating that degree of threat is learned. Our results demonstrate that degree of threat corresponds to neural activity in the auditory areas and that threat can be conveyed by different species signals and that these signals must be learned.

Biological relevance of acoustic signal affects discrimination performance in a songbird

The fee–bee song of the black-capped chickadee (Poecile atricapillus) is a two-note, tonal song that can be sung at different absolute pitches within an individual. However, these two notes are produced at a consistent relative pitch. Moreover, dominant birds more reliably produce songs with this species-typical interval, compared to subordinate birds. Therefore, we asked whether presenting the species-typical relative pitch interval would aid chickadees in solving pitch interval discriminations. We found that species-typical relative pitch intervals selectively facilitated discrimination performance using synthetic sine-wave stimuli. Using shifted fee–bee song notes from recordings of naturally produced songs, birds learned the discrimination in fewer trials overall compared to synthetic stimuli. These results may reflect greater generalization among stimuli that occur outside species-typical production parameters. In addition, although sex differences in performance are rarely observed in acoustic discriminations in chickadees, female chickadees performed more accurately compared to males.

Mechanisms of call note-type perception in black-capped chickadees (Poecile atricapillus): peak shift in a note-type continuum.

We report on operant conditioning and artificial neural network (ANN) simulations aimed at further elucidating mechanisms of black-capped chickadee chick-a-dee call note category perception. Specifically, we tested for differences in the speed of acquisition among different discrimination tasks and, in two selected discrimination groups, searched for evidence of peak shift. Earlier, unreported ANN data were instrumental in providing the motivation for the current set of studies with chickadees and are provided here. The ANNs revealed differences in the speed of learning among note-type discrimination groups that is related to the degree of perceptual similarity among the three note types tested (i.e., A, B, and C notes). In many respects, bird and network results were in agreement (i.e., in the observation of peak shift in the same group), but they also differed in important ways (i.e., all discrimination groups showed differences in speed of learning in simulations but not in chickadees). We suggest that the start, peak and end frequency of the chick-a portion of chick-a-dee call notes, which form a graded but overlapping continuum, may drive the peak shift observed.

ZENK Activation in the Nidopallium of Black-Capped Chickadees in Response to Both Conspecific and Heterospecific Calls

Neuronal populations in the songbird nidopallium increase in activity the most to conspecific vocalizations relative to heterospecific songbird vocalizations or artificial stimuli such as tones. Here, we tested whether the difference in neural activity between conspecific and heterospecific vocalizations is due to acoustic differences or to the degree of phylogenetic relatedness of the species producing the vocalizations. To compare differences in neural responses of black-capped chickadees, Poecile atricapillus, to playback conditions we used a known marker for neural activity, ZENK, in the caudal medial nidopallium and caudomedial mesopallium. We used the acoustically complex ‘dee’ notes from chick-a-dee calls, and vocalizations from other heterospecific species similar in duration and spectral features. We tested the vocalizations from three heterospecific species (chestnut-backed chickadees, tufted titmice, and zebra finches), the vocalizations from conspecific individuals (black-capped chickadees), and reversed versions of the latter. There were no significant differences in the amount of expression between any of the groups except in the control condition, which resulted in significantly less neuronal activation. Our results suggest that, in certain cases, neuronal activity is not higher in response to conspecific than in response to heterospecific vocalizations for songbirds, but rather is sensitive to the acoustic features of the signal. Both acoustic features of the calls and the phylogenetic relationship between of the signaler and the receiver interact in the response of the nidopallium.

Phonological perception by birds: budgerigars can perceive lexical stress

Metrical phonology is the perceptual “strength” in language of some syllables relative to others. The ability to perceive lexical stress is important, as it can help a listener segment speech and distinguish the meaning of words and sentences. Despite this importance, there has been little comparative work on the perception of lexical stress across species. We used a go/no-go operant paradigm to train human participants and budgerigars (Melopsittacus undulatus) to distinguish trochaic (stress-initial) from iambic (stress-final) two-syllable nonsense words. Once participants learned the task, we presented both novel nonsense words, and familiar nonsense words that had certain cues removed (e.g., pitch, duration, loudness, or vowel quality) to determine which cues were most important in stress perception. Members of both species learned the task and were then able to generalize to novel exemplars, showing categorical learning rather than rote memorization. Tests using reduced stimuli showed that humans could identify stress patterns with amplitude and pitch alone, but not with only duration or vowel quality. Budgerigars required more than one cue to be present and had trouble if vowel quality or amplitude were missing as cues. The results suggest that stress patterns in human speech can be decoded by other species. Further comparative stress-perception research with more species could help to determine what species characteristics predict this ability. In addition, tests with a variety of stimuli could help to determine how much this ability depends on general pattern learning processes versus vocalization-specific cues.

Dominance and geographic information contained within black-capped chickadee (Poecile atricapillus) song

In songbirds, male song is an acoustic signal used to attract mates and defend territories. Typically, song is an acoustically complex signal; however, the fee-bee song of the black-capped chickadee is relatively simple. Despite this relative simplicity, two previous studies (Christie et al., 2004b; Hoeschele et al., 2010) found acoustic features within the fee-bee song that contain information regarding an individual’s dominance rank; however each of these studies reported a different dominance-related acoustic cue. Specifically, the relative amplitude of the two notes differed between the songs of dominant and subordinate males from northern British Columbia, while the interval pitch ratio differed between the songs of dominant and subordinate males from eastern Ontario. In the current study, we examined six acoustic features within songs from both of the chickadee populations (northern British Columbia and eastern Ontario) examined in these previous studies and used bioacoustic analyses and discriminant function analyses to determine whether there is a consistent dominance-related acoustic cue across both, or in each of these populations. Consistent with the previous findings, the current results indicate that relative amplitude differs based on dominance status in the songs from British Columbia; however, our results failed to reach significance with songs from Ontario. These results suggest that acoustic cues that signal a male’s dominance in this species vary with geographic location. Furthermore, examining songs from these two locations and one additional location in northern British Columbia, we found that discriminant function analyses could correctly classify songs based on geographic location. Considering the broad extent of the species’ range, black-capped chickadee song is considered relatively invariant; however, our results suggest that there is geographic variation in songs, although the differences are subtle compared to geographic song variation in other species.

Acoustic mechanisms of a species-based discrimination of the chick-a-dee call in sympatric black-capped (Poecile atricapillus) and mountain chickadees (P. gambeli)

Previous perceptual research with black-capped and mountain chickadees has demonstrated that these species treat each others namesake chick-a-dee calls as belonging to separate, open-ended categories. Further, the terminal dee portion of the call has been implicated as the most prominent species marker. However, statistical classification using acoustic summary features suggests that all note-types contained within the chick-a-dee call should be sufficient for species classification. The current study seeks to better understand the note-type based mechanisms underlying species-based classification of the chick-a-dee call by black-capped and mountain chickadees. In two, complementary, operant discrimination experiments, both species were trained to discriminate the species of the signaler using either entire chick-a-dee calls, or individual note-types from chick-a-dee calls. In agreement with previous perceptual work we find that the D note had significant stimulus control over species-based discrimination. However, in line with statistical classifications, we find that all note-types carry species information. We discuss reasons why the most easily discriminated note-types are likely candidates to carry species-based cues.