Receivers respond differently to chick-a-dee calls varying in note composition in Carolina chickadees, Poecile carolinensis

The chick-a-dee call of the avian genus Poecile is a structurally complex vocal system because it possesses a set of simple rules that governs how the notes of the call are ordered, and variable numbers of each of the note types strung together can generate an extraordinary number of unique calls. Whereas it has been hypothesized that chick-a-dee calls with different notes may convey different information, no experimental evidence has been offered in support of the hypothesis. Previously published studies suggested that flock members use chick-a-dee calls in the context of moving to or from a feeding site. Here, we tested Carolina chickadees' responses to playbacks of chick-a-dee calls that differed in note composition. Playbacks were conducted in the field in the context of a novel food source. Our pilot data had indicated that chick-a-dee calls with relatively large numbers of ‘C’ notes were given by birds on their first contact with a novel seed stand. In the present study, we found that chickadees flew in close to the playback speaker and subsequently took seed from a seed stand more often during playbacks of chick-a-dee calls containing C notes than chick-a-dee calls not containing C notes or than control playbacks. Vocal responses of chickadees to the playbacks also differed in relation to the particular vocal signal being played back. These results indicate that receivers respond differently to chick-a-dee calls containing different compositions of note types and represent a first step to link variation in note composition and ordering in these calls to possible meanings.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Variation in Note Composition of Chick‐a‐dee Calls is Associated with Signaler Flight in Carolina Chickadees,Poecile carolinensis

Chick‐a‐dee calls are used in a wide range of social contexts in Poecile (chickadee) species. These calls comprise a number of distinct note types. Earlier naturalistic observational studies suggested that the ‘C’ note type was used frequently in calls of Carolina chickadees (P. carolinensis) in the context of flight. We conducted three field studies with Carolina chickadees to test in more experimentally manipulative ways whether Chick‐a‐dee calls with more ‘C’ notes were associated with flight. The three studies differed in how they elicited flight behavior from chickadees, as well as in the likely arousal levels experienced by the birds. First, we captured chickadees and released them, recording any calls they produced in flight or when later perched after escape. Second, we approached chickadees that were foraging near the ground in field settings and recorded any calls they produced when perched compared to when they were in flight. Third, from a distant blind, we recorded chickadees flying to and from feeding stations, in which the closest perching substrate/cover was at least 2 m away from the feeding station, thus requiring flight. In all three studies, calls contained more ‘C’ notes when birds were in flight compared to when they were perched. This work expands our understanding of variation in note composition of chick‐a‐dee calls beyond the contexts of food and predator detection to the context of movement. Studies are now needed to test whether such variation in chick‐a‐dee calls brings about group cohesion.     

Development of Early Vocalizations and the Chick-a-dee Call in the Black-capped Chickadee,Parus atricapillus

The chick-a-dee call of the black-capped chickadee (Parus atricapillus) is composed of discrete elements, or notes, that are combined to form hundreds of different calls. To investigate the development of this complex call, 12 families of color-marked chickadees were observed and recorded in the wild. Vocalizations were monitored for 18 d in the nest and 14–18 d postfledging. Most vocalizations of nestlings and fledglings were associated with feeding. At hatching, vocalizations consisted of a structurally simple note type that became more complex and variable with age. Around 9–12 d, the development of the call occurred, when single notes became organized into a multiple-note unit. Notes within the call differentiated into higher frequency, rapidly modulated initial note types and a lower frequency, moderately modulated terminal note type, features also present in adult chick-a-dee calls. Several adult-like calls including chick-a-dee calls, fee-bee songs, and a subsong-like vocalization developed prior to fledgling dispersal. Based on resemblances of note structure and general call structure, the chick-a-dee call appeared to develop from calls of nestlings and fledglings, although not necessarily in a chronologically linear progression. Some features of the chick-a-dee call closely resembled features of older nestling and fledgling calls, while other features more closely resembled the sounds of very young nestlings. Vocal development in the chickadee is compared with song and call development in other species, and the possible significance of acoustic resemblances between chick-a-dee calls and the food-associated calls of nestlings and fledglings is discussed.     

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. 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. 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. 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.     

Categorization and discrimination of "chick-a-dee" calls by wild-caught and hand-reared chickadees

Bloomfield and Sturdy [Bloomfield, L.L., Sturdy, C.B. All chick-a-dee calls are not created equally. Part I. Open-ended categorization by sympatric and allopatric chickadees. Behav. Proc., in press] previously reported that black-capped chickadees (Poecile atricapillus) discriminate conspecific from heterospecific (mountain chickadee, P. gambeli) 'chick-a-dee' calls, and their ability to accurately discriminate and classify the calls as belonging to separate species' defined categories was largely unaffected by their prior experience with mountain chickadees and their calls. To further examine the potential influence of experience on discrimination and categorization, we compare wild-caught black-capped chickadees, wild-caught mountain chickadees, and black-capped chickadees hand-reared among either adult laboratory-housed black-capped chickadees or adult laboratory-housed mountain chickadees on a true category/pseudo category chick-a-dee call discrimination task. Irrespective of group assignment, hand-reared birds performed as well as wild-caught birds and did not show a conspecific- or rearing-specific advantage in discrimination, categorization or memorization of chick-a-dee calls. While vocal learning is under the influence of ontogenetic experience, the results derived from the current methods suggest that experience (or a lack thereof) does not affect categorization and memorization abilities.     

Geographic Variation in Note Composition and Use of chick‐a‐dee Calls of Carolina Chickadees (Poecile carolinensis)

The aim of this study was to determine whether geographic variation exists in the composition of note types in the chick‐a‐dee call of Carolina chickadees. This determination is of interest for two reasons: earlier studies with a related species suggested minimal geographic variation in note composition, and geographic variation in social signals may represent important developmental or selection processes shaping signal use. Carolina chickadees were recorded in a naturalistic observation study in west‐central Indiana. Chick‐a‐dee calls were analyzed and compared to calls from an eastern Tennessee population that had been described in a previously published study (Auk, 125, 2008, 896). Despite much similarity in the basic rules by which notes are organized to compose calls, there were several significant differences in how calls of the two populations were structured. Furthermore, birds from Indiana used their chick‐a‐dee calls in certain contexts in different ways compared to birds from Tennessee. These findings suggest interesting population‐level variation in this call system, and future research should be able to determine whether these differences are driven by evolutionary, ecological, or developmental factors, or some combination of these factors.     

All "chick-a-dee" calls are not created equally. Part II. Mechanisms for discrimination by sympatric and allopatric chickadees

The 'chick-a-dee' call, common to all members of the genus Poecile, is used by both sexes throughout the year to putatively co-ordinate flock movements and register alarm. In some regions, two or more chickadee species occupy overlapping territories, and therefore it is essential that these sympatric species learn to discriminate between the acoustically similar calls of the species. Previous work from our laboratory has shown that black-capped (P. atricapillus) and mountain chickadees (P. gambeli) discriminate between the species' calls and treat each species' calls as belonging to separate open-ended categories. In the current set of experiments we use an operant conditioning paradigm to gain an understanding of (1) how the birds perform this discrimination and (2) whether birds with different levels of experience with heterospecific calls perform this task differently. We use natural recordings of chick-a-dee calls and perform several manipulations to test the importance of the introductory 'chick-a' portion and the terminal 'dee' portion for discriminating among the calls of the two species. Evidence suggests that birds mainly use the terminal 'dee' portion, as all groups of birds responded similarly to these probe stimuli and control chick-a-dee calls. We propose that the terminal 'dee' portion, consisting of lower frequency notes, is more likely to be resistant to degradation, and therefore a more reliable species-specific marker.     

Call-based species recognition in black-capped chickadees

Species recognition is essential for efficient communication between conspecifics. For this to occur, species information must be unambiguously encoded in the repertoire of each species’ vocalizations. Until now, the study of species recognition in songbirds has been focused mainly on male songs and male territorial behaviour. Species recognition of other learned vocalizations, such as calls, have not been explored, and could prove useful as calls are used in a wider range of contexts. Here, we present an experimental field study investigating the coding of species information in a learned vocalization, the ‘chick-a-dee’ call of the black-capped chickadee (Poecile atricapillus). By modifying natural calls in both temporal and spectral domains and by observing the vocal responses of black-capped chickadees following the playback of these modified calls, we demonstrate that species recognition in chickadees relies on several acoustic features including syntax, frequency modulation, amplitude modulation, and to a lesser extent, call rhythmicity and frequency range.     

Variation in chick‐a‐dee calls of bridled titmice (Baeolophus wollweberi): Frequent use of non‐combinatorial calls in a combinatorial calling system

Chick‐a‐dee calls of Poecile (chickadee) and Baeolophus (titmouse) species are complex in terms of the structural composition of note types and the diversity of messages. Studies so far have mainly focused on the calls of various chickadee and just one titmouse species—the tufted titmouse (B. bicolor). To begin to address this lack of titmouse data, our study investigated variation in note composition of calls of bridled titmice (B. wollweberi). We obtained calls from 26 flocks in the Chiricahua Mountains of Arizona in the overwintering flocking period. Bridled titmice produce proportionally more non‐combinatorial call variants than combinatorial call variants. The number of the single noted calls furthermore exceeded the number of multinote calls. In general, structural variation in the combinatorial calls appears to be comparable to calls of better‐studied chickadees and of tufted titmice, although bridled titmice appear to have a unique call length distribution. We also analyzed some behavioral associations with call variation and found that flight behavior and close interactions between individuals were associated with use of specific note types. Finally, we found microgeographic variation in note type use in these calls. We discuss some possible explanations for call complexity in this species.     

Differential Response to Interspecific and Intraspecific Signals Amongst Chickadees

Black‐capped chickadees (Poecile atricapillus) and mountain chickadees (P. gambeli) have a similar vocal repertoire and share many other life history traits; yet, black‐capped chickadees are socially dominant to mountain chickadees where populations overlap. Previous research suggested that in contact zones, both species respond weakly to heterospecific songs during the breeding season, and have suggested minimal interspecific competition. However, both black‐capped and mountain chickadees discriminate between conspecific and heterospecific chick‐a‐dee calls, suggesting attention is paid to interspecific signals. We compared the responses of both black‐capped and mountain chickadees to conspecific and heterospecific chick‐a‐dee calls during the winter, when both species compete for the same food resources. We conducted an aviary playback experiment exposing both species to playback composed of heterospecific and conspecific chick‐a‐dee calls, which had been recorded in the context of finding food sources. Responses from the tested birds were measured by recording vocalizations and behaviour. Black‐capped chickadees responded significantly more to conspecific than to heterospecific stimuli, whereas the subordinate mountain chickadees responded to both mountain and black‐capped chickadee calls. Based upon the reactions to playbacks, our results suggest these two closely related species may differ in their perception of the relative threat associated with intra‐ versus interspecific competitors.     

Syntactical Organization of the Gargle Vocalization of the Black-capped Chickadee,Parus atricapillus

The gargle is a complex call of the black-capped chickadee Parus atricapillus associated with agonistic interactions. A large sample of calls was recorded from five sites in southeastern Wisconsin. Three sites were near one another and the other two with a different dialect pattern were more distant (all sites were within 15 km of each other). A typical call consists of about 6 notes selected from an array of about 15 different note-types that are shared among individuals in the same population. Note-types are given in many combinations, and any individual may deliver many different variations. Analysis of two- and three-note sequences shows a syntactical organization with certain note-types much more likely to precede or follow than others. In some cases linkage between note-types was nearly complete. Some differences occurred among individuals and sites, but general organizational rules were similar. One effect on ordering was acoustical structure of the notes. Higher pitched, shorter duration notes were more likely at the beginning than the end of the call which often consisted of trills. Organization of the gargle was compared to that of the chick-a-dee call of the same species. Similarities include recombinant properties, general acoustic rules and syntax. A major difference may be that in chick-a-dee calls various note combinations constituting a call have different meanings, while the various note combinations comprising an individual's repertoire of gargles may be functionally equivalent.     

All "chick-a-dee" calls are not created equally. Part I. Open-ended categorization of chick-a-dee calls by sympatric and allopatric chickadees

Researchers trained 24 black-capped (Poecile atricapillus) and 12 mountain (P. gambeli) chickadees in an operant conditioning task to determine if they use open-ended categorization to classify "chick-a-dee" calls, and whether black-capped chickadees that had experience with mountain chick-a-dee calls (sympatric group) would perform this task differently than inexperienced black-capped chickadees (allopatric group). All experimental birds learned to discriminate between species' call categories faster than within a category (Experiment 1), and subsequently classified novel and original between-category chick-a-dee calls in Experiments 2 and 3 following a change in the category contingency. These results suggest that regardless of previous experience, black-capped and mountain chickadees classify their own and the other species' calls into two distinct, yet open-ended, species-level categories.     

Call Learning in Black-capped Chickadees (Parus atricapillus): The Role of Experience in the Development of ‘Chick-A-Dee’ Calls

The role of learning in the development of bird vocalizations other than territorial song is not well studied. The well-known role of direct imitation in the development of territorial song potentially masks the effects of other processes in the development of vocal behaviour. The ‘chick-a-dee’ call of black-capped chickadees is a good system in which to investigate more subtle developmental processes because this call is composed of a small number of distinctive note types. These note types may be classified objectively based on a simple set of acoustic variables, allowing for a quantitative assessment of vocal learning. We raised four groups of black-capped chickadees under different degrees of social and acoustic isolation. We then used a multivariate analysis of the acoustic structure of the introductory call notes (‘A-’ ‘B-’ and ‘C-notes’) to determine how similar the notes produced by these hand-reared birds were to the notes of wild birds. Hand-reared chickadees with greater exposure to normal phonology produced notes of all three note types that were more similar to those of wild birds. Regardless of experience, however, all birds produced A-notes that fell within the normal range of those produced by wild birds. By contrast, the development of normal B- and C-notes appears to be more dependent upon experience. These data suggest that learning may play a different role in the development of different phonological units within one vocalization. Our results also illustrate the importance of considering processes other than simple imitation in the development of avian vocalizations.     

Pitch-related cues in the songs of sympatric mountain and black-capped chickadees

Acoustic frequency (pitch) cues are known to be important in the recognition of conspecific song in a number of songbird species. Mountain chickadees (Poecile gambeli) and black-capped chickadees (Poecile atricapillus) are sympatric over parts of their ranges and their species-typical songs share many features. I examined the acoustic characteristics of song of these two congeners in a region of sympatry in southern Alberta, Canada. As reported for other populations in allopatry, black-capped chickadees emphasized relative frequency cues in song production. In particular, variation in the ratios between note frequencies was significantly less than variation in the note frequencies themselves. In contrast, songs of mountain chickadees did not have constant frequency ratios and contained an introductory acoustic element absent in black-capped chickadee song. Both species may rely on song note frequency or the presence of this introductory acoustic element when differentiating between conspecific song and heterospecific song. Song measures for chickadees in sympatry were similar to measures in allopatry, providing little evidence for character displacement in song production.     

Constraints on the Structure of Combinatorial “Chick-a-dee” Calls

“Chick-a-dee” calls of the black-capped chickadee (Parus atricapillus) constitute a combinatorial system of animal communication, apparently the only such system yet described. Four note-types, which may be omitted or repeated a variable number of times, occur in a fixed sequence (A–B–C–D) to constitute calls. Quantitative analyses determining the nature of departures from first-order transitional probabilities between successive notes revealed a variety of results that point consistently to two underlying features of calls. (1) Some constraint operates to limit the length of calls, as manifest in shortening of repetition-strings and omitting of note-types expected to follow. (2) There is an opposing tendency to include at least one or two D-notes at the end of a call, regardless of the overall length. The second feature suggests important semantic properties of D-notes, especially the ratio of D s to other note-types and the flock-specific acoustical structure of D-notes. The constraint on length of call does not appear intimately related to semantic causes, but may instead be determined by the maximum duration of continuous phonation, in parallel with the fundamental breath-group of human speech. In this respect, a “chick-a-dee” call resembles an entire “natural sentence” of spoken human language.     

Response of Captive Raptors to Avian Mobbing Calls: the Roles of Mobber Size and Raptor Experience

The ‘move on’ hypothesis for avian mobbing proposes that mobbing induces stress in potential predators, thereby provoking them into moving elsewhere. We tested whether mobbing is stress inducing by subjecting captive owls, hawks, and falcons to the mobbing calls of four species of co‐occurring passerine birds that vary considerably in body size. Test subjects comprised 15 individuals of seven species of birds of prey that were housed at a wildlife rehabilitation center in northwestern Pennsylvania, USA. Playback treatments included mobbing calls of the black‐capped chickadee (Poecile atricapillus), blue‐headed vireo (Vireo solitarius), blue jay (Cyanocitta cristata), and American crow (Corvus brachyrhynchos), which vary in size from 12 g (chickadee) to 500 g (crow). A non‐mobbing vocalization (song of the black‐capped chickadee) was included in the playback treatments as a control. Playback treatment produced pronounced effects on three behavioral indicators of probable stress: head orientation toward the playback speaker, raising of feathers or spreading of wings, and changing of perch positions. Test subjects responded more vigorously to mobbing calls of the large passerines (jays and crows) than to those of the smaller passerines (chickadees and vireos). In addition, raptors that had entered the rehabilitation facility as adults generally responded more vigorously to the mobbing calls of jays and crows than did naive individuals that had entered the facility as fledglings or young juveniles. Our results are therefore consistent with the ‘move on’ hypothesis and suggest (1) that the mobbing calls of large passerines are more effective in provoking stress and altering the behavior of potential predators than are the mobbing calls of small passerines and (2) that a raptor's previous experience with mobbing in the wild can exaggerate the strength of its response, particularly to the mobbing calls of large passerines.     

Traffic noise and responses to a simulated approaching avian predator in mixed-species flocks of chickadees,titmice, and nuthatches

Traffic noise likely reaches a wide range of species and populations throughout the world, but we still know relatively little about how it affects anti-predator behavior of populations. We tested for possible effects of traffic noise on responses to predator acoustic cues in Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis) near 14 independent feeding stations in eastern Tennessee. We compared anti-predator calling and seed-taking behavior in response to playbacks of predator stimuli (screech owl calls) at sites naturally exposed to traffic noise and at sites that faced relatively little traffic noise. The screech owl call playback was designed to simulate the approach of this dangerous predator to a feeder being used by these small songbirds. We found that chickadees responded consistently to the owl stimuli across different levels of traffic noise. However, titmice, and nuthatches exhibited different behavioral responses to the predator stimulus, suggesting that traffic noise masked these low-frequency predator calls. Overall, chickadees and nuthatches showed the broadest anti-predator behavioral responses in comparison to titmice, corroborating earlier published work with an Indiana population. Finally, populations exposed to traffic noise overall seemed less able to detect predator cues potentially masked by that noise, and future work will need to assess likely seasonal variation in these responses as well as species-level variation in anti-predator responses in mixed-species groups.     

Vocal communication in a neotropical treefrog, Hyla ebraccata: Advertisement calls

We studied the vocal communication of Hyla ebraccata in central Panama. The advertisement call of this species consists of a pulsed buzz-like primary note which may be given alone or followed by 1–4 secondary click notes. Primary notes are highly stereotyped, showing little variation within or0 among individuals in dominant frequency, duration, pulse repetition rate or rise time. Males calling in isolation give mostly single-note calls. They respond to playbacks of conspecific calls by increasing calling rates and the proportion of multi-note calls, and by giving synchronized calls 140–200 ms after the stimulus begins. Responses to conspecific advertisement calls are usually given immediately after the primary note of the leading call, but the primary note of the response often overlaps with the click notes of the leading call. Experiments with synthetic signals showed that males synchronize to any type of sound of the appropriate frequency (3 kHz), regardless of the fine structure of the stimulus. Playbacks of synthetic calls of variable duration showed that males do not synchronize well to calls less than 150 ms long, but they do to longer calls (200–600 ms). The variance in response latency increased with increasing stimulus duration, but modal response times remained at around 140–200 ms. Similar results were obtained in experiments withsynthetic calls having a variable number of click notes. Males showed no tendency to increase the number of click notes in their calls in response to increasing stimulus duration or increasing number of clicks in the stimulus. Females preferred three-note to one-note calls in two-choice playback experiments, whether these were presented in alternation, or with the one-note call leading and the three-note call following. Females showed no preference for leader or follower calls when both were one-note. When two-note calls were presented with the primary note of the follower overlapping the click note of the leader, females went to calls in which click notes were not obscured. Our results indicate that male H. ebraccata respond to other males in a chorus in ways which enhance their ability to attract mates.     

Two Novel Vocalizations Are Used by Veeries (Catharus fuscescens) during Agonistic Interactions

Avian vocalizations are common examples of the complex signals used by animals to negotiate during agonistic interactions. In this study, we used two playback experiments to identify agonistic signals in a songbird species with several acoustically complex songs and calls, the veery. In the first experiment, we compared veery singing behavior in response to simulated territorial intrusions including playback of three variations of veery song: 1) song alone as a control, 2) songs with added whisper calls, and 3) songs with introductory notes removed. In the second experiment, we used multimodal stimuli including songs, whisper calls and songs with introductory notes removed, along with a robotic veery mount. Focal males readily responded to all of the playback stimuli, approached the speaker and/or robotic mount, and vocalized. Male veeries gave more whisper calls, and sang more songs without the introductory note in response to all types of playback. However, veeries responded similarly to all types of stimuli presented, and they failed to physically attack the robotic mount. These results indicate that rival veeries use two different types of novel vocalizations: whisper calls and songs lacking the introductory note as agonistic signals, but do not allow us to discern the specific functions of these two vocalizations.     

Variable effect of playback of chickadee mobbing calls on detection probability of boreal forest birds

Modification of the point count survey method to include playback of songbird mobbing calls in an attempt to increase detection probabilities has met with mixed success. We compared detection probabilities for boreal forest songbirds using traditional point count methods and counts using broadcasts of the mobbing calls of Black‐capped Chickadees (Poecile atricapillus) in an attempt to increase detection probability. We conducted 594 point counts during the 2010 breeding season in Newfoundland, Canada. Each point count consisted of an 8‐min silent observation period followed by an 8‐min broadcast of Black‐capped Chickadee mobbing calls. Occupancy model results showed that response to playback broadcast varied across species, with detection probabilities higher for seven of 17 species during the silent portions of point counts and three species more likely to be detected during playback intervals. For all species, the number of visual detections increased during periods of playback and, averaged across species, individuals were >6 times more likely to be seen during the playback period than during the silent period. Differences in detection probability among observers were apparent during both silent and playback periods. We suggest that using playback of chickadee mobbing calls during point count surveys of common boreal forest songbird species may be most beneficial when visual detection is important. However, playback may also be useful for species‐specific surveys during periods when birds are less likely to be vocal or for studies of less common species with chronically low detection probabilities. A combined silent and playback approach could also be useful, although observer and species differences should be accounted for if comparing data across species or studies.