VOCAL ONTOGENY OF NESTLING AND FLEDGLING BLACK-CAPPED CHICKADEES POECILE ATRICAPILLA IN NATURAL POPULATIONS

ABSTRACT

We studied the vocal ontogeny of black-capped chickadees Poecile atricapilla from hatching through approximately age 40 days, at which time the juveniles dispersed from their hatching area. Development of three vocalisations (chick-a-dee call, fee-bee song, gargle call) was monitored by tape recording daily. Spectrographs quantification and comparison were carried out with Sound Analysis software. Developmental changes in offspring vocalisations were compared to the parent birds, allowing a measure of acoustic similarity between adults and young throughout early life. The chick-a-dee call developed all four of its component syllables (ABCD) from a single sound of day-old nestlings, but the four syllables emerged in adult form at different times in ontogeny. The fee-bee song was produced in impressively adult form starting at about age 20 days, with no precursor sounds to indicate gradual emergence. The principal difference between adult and juvenile fee-bee songs was the persistent production of three or four notes by juveniles rather than the adults' species-typical two notes. Gargle calls appear to develop from “subsong” strings of precursor gargle syllables. Juvenile gargles began to be identifiable at about age 33–35 days but did not match any of the gargle calls of the local adult population. Post-dispersal juveniles may develop gargles that match the gargle types of local birds where they settle.     

Family- and sex-specific vocal traditions in a cooperatively breeding songbird

Although songbirds provide well-known examples of cultural transmission of vocalizations, little is known about this process in species that live in stable social groups. Here I describe complex vocal traditions in a cooperatively breeding songbird, the stripe-backed wren (Campylorhynchus nuchalis). Repertoires of stereotyped calls were recorded from individually marked males and females in cooperative family groups. Males in the same patriline, whether in the same group or in different groups, had call repertoires that were nearly identical. Females in the same matriline also had identical call repertoires; however, female calls never matched the calls of males in the same group or in any nearby groups. Unrelated birds almost never shared calls. Call repertoires are apparently learned preferentially from same-sex relatives within family groups, so that call traditions separately follow patrilines and matrilines. This unique pattern of transmission results in vocal cues that reflect both sex and kinship.     

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.     

Call Convergence within Groups of Female Budgerigars (Melopsittacus undulatus)

The budgerigar (Melopsittacus undulatus) is a promising model species for the study of adult vocal learning. To date, several studies have confirmed the existence of vocal plasticity and, more importantly, rapid imitation of contact calls by adult male budgerigars. Vocal learning has not been investigated in female budgerigars, however. Since one likely function of the contact call is to denote group affiliation, we tested the hypothesis that female budgerigars, when placed into groups, would develop a shared contact call. We recorded the contact call repertoires of eight adult female budgerigars that were unfamiliar with one another, then placed them into two groups. Each group was deprived of visual contact with other birds. Recording sessions continued for the subsequent 8 wks, and behavioral observations were also conducted during this time. Within 4–7 wks, females in both groups converged on a common call type. This rate of convergence is slower than that observed in prior experiments limited to male birds, and much slower than vocal imitation by male budgerigars paired with females. Therefore, while our study documents vocal plasticity in adult female budgerigars, it also suggests that female budgerigars learn new vocalizations more slowly than males do.     

A comparative study of avian auditory brainstem responses: correlations with phylogeny and vocal complexity, and seasonal effects

We conducted a comparative study of the peripheral auditory system in six avian species (downy woodpeckers, Carolina chickadees, tufted titmice, white-breasted nuthatches, house sparrows, and European starlings). These species differ in the complexity and frequency characteristics of their vocal repertoires. Physiological measures of hearing were collected on anesthetized birds using the auditory brainstem response to broadband click stimuli. If auditory brainstem response patterns are phylogenetically conserved, we predicted woodpeckers, sparrows, and starlings to be outliers relative to the other species, because woodpeckers are in a different Order (Piciformes) and, within the Order Passeriformes, sparrows and starlings are in different Superfamilies than the nuthatches, chickadees, and titmice. However, nuthatches and woodpeckers have the simplest vocal repertoires at the lowest frequencies of these six species. If auditory brainstem responses correlate with vocal complexity, therefore, we would predict nuthatches and woodpeckers to be outliers relative to the other four species. Our results indicate that auditory brainstem responses measures in the spring broadly correlated with both vocal complexity and, in some cases, phylogeny. However, these auditory brainstem response patterns shift from spring to winter due to species-specific seasonal changes. These seasonal changes suggest plasticity at the auditory periphery in adult birds.     

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 .     

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.     

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.     

Cultural transmission of vocalizations in ravens, Corvus corax

As ravens have pronounced learning capabilities, especially in the vocal domain, cultural transmission might be a relevant factor affecting the composition of their vocal repertoires. We investigated how important cultural transmission is in establishing a raven's vocal repertoire and whether there are different pathways of transmission. We studied individually known free-ranging breeding pairs whose vocalizations were recorded during interactions with a caged pair. The mean repertoire size of these vocalizations was 12 call types per individual (from 79 types recorded from 74 individuals), with no difference between the sexes. In 81% of individuals the repertoire was composed entirely of calls also used by other individuals. Analysis of the distribution of call types among individuals regarding sex, partnership and neighbourhood and aspects of the geographical distribution of calls showed that the main pathway of cultural transmission was within the sexes. In addition, transmission occurred between pair partners, as well as between neighbouring and more distant pairs. About 40% of the calls in a raven's repertoire were transmitted within a sex and 10% between pair partners. Any two given birds in the population shared on average 20% (0-77%) of their calls. Cultural transmission within the sexes led to a pronounced sexual dimorphism in vocal behaviour. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Male and female rufous‐and‐white wrens do not match song types with same‐sex rivals during simulated territorial intrusions

In birds with song repertoires, song‐type matching occurs when an individual responds to another individual's song by producing the same song type. Song‐type matching has been described in multiple bird species and a growing body of evidence suggests that song‐type matching may serve as a conventional signal of aggression, particularly in male birds in the temperate zone. Few studies have investigated song‐type matching in tropical birds or female birds, in spite of the fact that avian biodiversity is highest in the tropics, that female song is widespread in the tropics, and that female song is the ancestral state among songbirds. In this study of rufous‐and‐white wrens Thryophilus rufalbus, a resident neotropical songbird where both sexes sing, we presented territorial males and females with playback that simulated a territorial rival producing shared and unshared songs. In response, both males and females sang matched song types at levels statistically equal to levels expected by chance. Furthermore, males and females exhibited similar levels of aggression and similar vocal behaviours in response to playback of both shared and unshared songs. These results indicate that rufous‐and‐white wrens do not use song‐type matching in territorial conflicts as a conventional signal of aggression. We discuss alternative hypotheses for the function of song‐type sharing in tropical birds. In particular, we point out that shared songs may play an important role in intra‐pair communication, especially for birds where males and females combine their songs in vocal duets, and this may supersede the function of song‐type matching in some tropical birds.     

Vocal plasticity in mallards: multiple signal changes in noise and the evolution of the Lombard effect in birds

Signal plasticity is a building block of complex animal communication systems. A particular form of signal plasticity is the Lombard effect, in which a signaler increases its vocal amplitude in response to an increase in the background noise. The Lombard effect is a basic mechanism for communication in noise that is well‐studied in human speech and which has also been reported in other mammals and several bird species. Sometimes, but not always, the Lombard effect is accompanied by additional changes in signal parameters. However, the evolution of the Lombard effect and related vocal adjustments in birds are still unclear because so far only three major avian clades have been studied. We report the first evidence for the Lombard effect in an anseriform bird, the mallard Anas platyrhynchos. In association with the Lombard effect, the fifteen ducklings in our experiment also increased the peak frequency of their calls in noise. However, they did not change the duration of call syllables or their call rates as has been found in other bird species. Our findings support the notion that all extant birds use the Lombard effect to solve the common problem of maintaining communication in noise, i.e. it is an ancestral trait shared among all living avian taxa, which means that it has evolved more than 70 million yr ago. At the same time, our data suggest that parameter changes associated with the Lombard effect follow more complex patterns, with marked differences between taxa, some of which might be related to proximate constraints.     

Song convergence in multiple urban populations of silvereyes (Zosterops lateralis)

Recent studies have revealed differences between urban and rural vocalizations of numerous bird species. These differences include frequency shifts, amplitude shifts, altered song speed, and selective meme use. If particular memes sung by urban populations are adapted to the urban soundscape, "urban-typical" calls, memes, or repertoires should be consistently used in multiple urban populations of the same species, regardless of geographic location. We tested whether songs or contact calls of silvereyes (Zosterops lateralis) might be subject to such convergent cultural evolution by comparing syllable repertoires of geographically dispersed urban and rural population pairs throughout southeastern Australia. Despite frequency and tempo differences between urban and rural calls, call repertoires were similar between habitat types. However, certain song syllables were used more frequently by birds from urban than rural populations. Partial redundancy analysis revealed that both geographic location and habitat characteristics were important predictors of syllable repertoire composition. These findings suggest convergent cultural evolution: urban populations modify both song and call syllables from their local repertoire in response to noise.     

Annual cycle of the black‐capped chickadee: Seasonality of singing rates and vocal‐control brain regions

Black‐capped chickadees have a rich vocal repertoire including learned calls and the learned fee‐bee song. However, the neural regions underlying these vocalizations, such as HVC, area X, and RA (robust nucleus of arcopallium), remain understudied. Here, we document seasonal changes in fee‐bee song production and show a marked peak in singing rate during March through May. Despite this, we found only minimal seasonal plasticity in vocal control regions of the brain in males. There was no significant effect of time of year on the size of HVC, X, or RA in birds collected in January, April, July, and October. We then pooled birds into two groups, those with large testes (breeding condition) and those with small testes (nonbreeding), regardless of time of year. Breeding birds had slightly larger RA, but not HVC or X, than nonbreeding birds. Breeding birds had slightly larger HVC and RA, but not X, as a proportion of telencephalon volume than did nonbreeding birds. Birds collected in July had heavier brains than birds at other times of year, and had the greatest loss in brain mass during cryoprotection. The absence of any overall seasonal change in the vocal‐control regions of chickadees likely results from a combination of individual differences in the timing of breeding phenology and demands on the vocal‐control regions to produce learned calls year‐round. © 2006 Wiley Periodicals, Inc. J Neurobiol, 2006     

Syllable sharing and changes in syllable repertoire size and composition within and between years in the great reed warbler, Acrocephalus arundinaceus

The syllable repertoire size of the great reed warbler (GRW) is known to underlay female preferences. However, its stability over a season—a key factor of this quality-related feature—has never been tested. Similarly, syllable repertoire composition, syllable sharing and its function in GRW have received little attention so far. GRW syllables fit into two categories: whistles and rattles. They differ in structure but nothing is known about their function. In the present study we analyze the above aspects of GRW vocalization. We found that syllable repertoire size and composition were stable within a season but significantly changed between years. Longitudinal analyses revealed that the changes in repertoire size were influenced more by the season than the age of individuals. The repertoire size correlated with harem size. Changes in repertoire size were significantly smaller than changes in composition, indicating varying seasonal usage of syllables present in the repertoires of individual birds. Syllable sharing was high and indifferent between neighbors and distant males. This pattern suggests that syllable sharing in GRW acts as a dialect. High levels of within- and between-season repertoire similarity among all recorded birds supported this view. Whistles were more shared and repeatable within and between seasons than rattles. We suppose that whistles may play an important role in determining a local dialect due to their lower changeability both between individuals and years. Within-season similarity of whistle repertoire to other males correlated with harem size, but similarity of rattle repertoire did not. This correlation may result from a female preference for philopatric males using the local dialect.     

Macrogeographic variation in the call of the corncrake Crex crex

This study was conducted to characterise macrogeographic variation in the vocalisation of the corncrake Crex crex, a bird species with a non‐learned and highly stereotyped call. We also examined: 1) whether call characteristics remained stable across successive breeding seasons within two of the study populations and 2) whether call similarity was related to distance between populations. Recordings of 352 males from eight populations were analysed. The analyses focused on variation in 1) temporal characteristics (duration of syllables and intervals, duration of the intervals between consecutive maximal amplitude peaks within syllables, called pulse‐to‐pulse duration (PPD)), and 2) spectral characteristics (minimal and maximal frequency, frequencies below which 25%, 50% and 75% acoustic energy of signal is distributed). We found significant differences in most of the temporal and all of the spectral characteristics between populations. No differences were found in PPD. Significant interannual differences in spectral characteristics were found in both of the populations examined, whereas differences in temporal characteristics were only observed in one population. In general, geographic variation in calls showed clinal distance‐dependence, where distant populations showed larger differences in call than neighbouring populations. Our results show that geographic variation in corncrake calls may be very dynamic in the short term and that within‐population variation may occur on the same scale as between‐population variation. This finding is surprising because call characteristics in non‐learners are essentially inherited, and genetic transmission should be very slow. We suggest that the social interactions between males and/or the specific dispersal patterns of this species and the low site fidelity of adult and young birds may be responsible for such pattern.     

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.     

Variation in Avian Vocalizations during the Non‐Breeding Season in Response to Traffic Noise

Low‐frequency traffic noise that leads to acoustic masking of vocalizations may cause birds to alter the frequencies or other components of their vocalizations in order to be heard by conspecifics and others. Altering parts of a vocalization may result in poorer vocal performance or the message contained in the vocalization being received incorrectly. During the winters of 2011–2012 and 2012–2013, we recorded and measured the ‘chick‐a‐dee’ call of Black‐capped Chickadees (Poecile atricapillus) and the ‘po‐ta‐to‐chip’ call of American Goldfinches (Spinus tristis) to determine whether components of the calls produced in areas of high traffic noise and low traffic noise differed in any way. We found that both chickadee and goldfinch calls had higher minimum frequencies in areas with high traffic‐noise than in low traffic‐noise areas. The maximum frequencies showed no differences in either species' calls. This suggests that chickadees and goldfinches alter the part of their calls that are acoustically masked by traffic noise in effort to better transmit the vocalization. These differences suggest that increasing anthropogenic noise may influence avian communication and that noise management should be included in conservation planning.     

Seasonal variation of vocal behaviour in a temperate songbird: assessing the effects of laboratory housing on wild-caught, seasonally breeding birds

Many laboratories are conducting research using songbirds as their animal model. In particular, songbirds are widely used for studying the behavioural and neural mechanisms underlying vocal learning. Many researchers use wild-caught birds to conduct this research, although few studies of behaviour have been conducted to determine the effects of captive housing on these species. We investigated the vocal production pattern of wild-caught black-capped chickadees (Poecile atricapillus) over an entire season in laboratory housing. We documented the frequency of production of four vocalizations (fee-bee song, chick-a-dee calls, dee calls, and gargle calls) across seasons and diurnal pattern and compared the observed pattern of laboratory vocalizations to those previously observed and reported in the wild. Laboratory-housed chickadees had seasonal and diurnal vocal production shifts that were related to both photoperiodic changes (season) and diurnal pattern. For instance, there was significantly more fee-bee song in the spring than summer, autumn, and winter with the most fee-bee song occurring at spring dawn as seen in the wild. Our results also confirmed that the general pattern of vocalizations was consistent between wild and laboratory populations, with no significant differences for either the seasonal or diurnal pattern of fee-bee song production between populations. Differences between settings were observed in the pattern of chick-a-dee calls at dawn and sunset between field and laboratory populations. However, differences in the quantity of vocalization types between laboratory and wild populations suggest that housing conditions are influencing the normal vocal behavioural patterns.