Behavioral Ecology Advance Access originally published online on September 24, 2008
Behavioral Ecology 2009 20(1):111-116; doi:10.1093/beheco/arn121
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Chick-a-dee call variation in Carolina chickadees and recruiting flockmates to food
a Department of Psychology b Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA
Address correspondence to T.M. Freeberg, Department of Psychology, 301B Austin Peay Building, University of Tennessee, Knoxville, TN 37996, USA. E-mail: tfreeber{at}utk.edu.
Received 12 June 2008; revised 8 August 2008; accepted 8 August 2008.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The "chick-a-dee" call of many Paridae species (titmice, tits, and chickadees) is structurally complex and functions in social cohesion. Studies with different Parid species suggest that variation in the note composition of calls relates to a wide variety of contexts. An earlier study with Carolina chickadees (Poecile carolinensis), the focal species of the present study, found that receivers responded differently to playback calls differing in note composition in feeding contexts. Here, we addressed whether signalers actually produce calls differing in note composition in feeding contexts and whether those calls might serve a recruitment function. In a first study, we found that the first chickadee to take seed from a feeding station produced calls with a greater number of D notes before the second chickadee arrived to take seed, compared with after the second chickadee arrived to take seed. This suggests that calls with a large number of D notes might serve a general recruitment function. We tested this idea in a second study, using playbacks of calls containing a large number of D notes or a small number of D notes at different sites. We found that the latency for a first chickadee to come into a site and take seed was shorter for playback variants containing a large number of D notes. Thus, in Carolina chickadees, chick-a-dee calls containing a large number of D notes may function to recruit other flock members to a discovered food source.
Key words: Carolina chickadee, chick-a-dee calls, foraging, recruitment, vocalizations.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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A major benefit of living in a social group is an increased ability to detect and exploit food resources (Wilson 1975
; Krause and Ruxton 2002). This ability is facilitated by vocal signaling in many species (Hauser 1996; Bradbury and Vehrencamp 1998). Communication about food presence with vocalizations has been documented in several taxa, including bats, cetaceans, primates, and birds (e.g., Elgar 1986; Heinrich 1988; Chapman and Lefebvre 1990; Hauser et al. 1993; Caine et al. 1995; Wilkinson and Boughman 1998; Evans and Evans 1999; Janik 2000; Di Bitetti 2005).
In black-capped chickadees, Poecile atricapillus, individuals finding a food source often produce chick-a-dee calls (Ficken 1981), which may function to recruit flock members. The chick-a-dee call of the avian subgenus Poecile is structurally complex and is produced in a variety of contexts related to social cohesiveness and interaction (Smith 1972; Ficken et al. 1978; Hailman et al. 1985; Hailman 1989; Smith 1991; Lucas and Freeberg 2007). The most extensive work on chick-a-dee call structure has been conducted with black-capped chickadees. The call in this species is composed of a small number of distinct note types that may be produced a varied number of times within any given call and that follow note ordering rules (Hailman et al. 1985, 1987; Charrier et al. 2004). The chick-a-dee call in Carolina chickadees, P. carolinensis, the focal species of the current study, is structurally similar to that of black-capped chickadees but appears to have a larger number of distinct note types (Bloomfield et al. 2005; Figure 1).
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It has been suggested that chick-a-dee calls differing in note composition could convey different messages (Hailman et al. 1985
; Hailman and Ficken 1986), but there has been little playback work to test this hypothesis. Templeton et al. (2005) found that captive black-capped chickadees produced calls with a greater number of D notes when they detected smaller and more threatening avian predators than when they detected larger and less threatening predators. In addition, playbacks of chick-a-dee calls varying in note composition produced mobbing-like behavior in receivers that was predictive of predator size. Freeberg and Lucas (2002) found that Carolina chickadees were more likely to come into feeding stations and take seed with playback calls that had a relatively large number of C notes compared with playback calls that had no C notes and a relatively large number of D notes. The Freeberg and Lucas (2002) study, however, did not distinguish calling during initial food detection from subsequent calling with regard to the number of C and D notes. In her seminal monograph on the vocal behavior of Carolina chickadees, Smith (1972, pp. 50–51) suggested that both C and D note usages may increase in the context of signalers flying to and departing from feeding stations when taking food from those stations. Thus, it is still rather an open question as to whether C notes or D notes, or perhaps both, might function in general recruitment or in recruitment specifically related to predator or food detection in chickadees. We conducted 2 studies to determine whether Carolina chickadees produce calls varying in C and D note composition when first detecting and exploiting a food source and, if so, if playbacks of calls varying in such note composition might serve to recruit other chickadees. In our first study, we recorded color-marked individuals at several field sites to determine whether the first chickadee to obtain seed from a feeding station produced calls with different note composition prior to a second chickadee taking seed from that feeding station, compared with after the second chickadee took seed from the feeding station. In our second study, we played back chick-a-dee calls that varied in note composition (based on results of the first study) to test whether calls differing in note composition might affect the latencies of receivers to take seed from feeding stations.
Based on earlier studies, we had specific expectations about 2 of the note types in chick-a-dee calls. First, D notes should occur less often in calls produced in food-related contexts if larger numbers of D notes are related to antipredator mobbing behavior (Templeton et al. 2005). However, D notes should occur more often in calls of a signaler that has detected a food source if these notes serve a more general recruitment function than solely predator mobbing. Second, C notes should be produced in greater numbers in calls in the context of discovering a food source if larger numbers of C notes are associated with food presence (as in Freeberg and Lucas 2002). However, if C notes are related more to the flight behavior of the signaler, as suggested by other studies (e.g., Smith 1972; Freeberg forthcoming) or to the detection of predators (e.g., Ficken et al. 1994), then usage of C notes may not be affected by initial contact with a food source.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study 1. Do birds vary note composition of calls when they detect food?
Study location
We recorded Carolina chickadees at the University of Tennessee Forest Resources, Research, and Education Center (36 N 00, 84 W 13). Recordings took place at these sites in the context of feeding stations, each made of a wooden board (25 cm x 40 cm x 2 cm) mounted atop a steel pole (1.8 m tall); when the pole was set in the ground, the board was roughly 1.5 m high. Each site was stocked every 10–14 days during the late fall and winter months with approximately 100 g of an equal amount of black oil sunflower and safflower seed to get the birds accustomed to the feeding stations as an irregular food source.
Recordings
Birds were recorded between 07:45 and 12:30 Eastern Standard Time in late winter and early spring months. After the observer arrived at a site and set up the recording equipment, the feeding station was stocked with roughly 50 g of a 1:1 mix of sunflower and safflower seed. The observer sat partially concealed behind vegetation or behind a camouflage fence blind 10 m from the feeding station and waited for chickadees to approach. Recording commenced when a Carolina chickadee first approached within 20 m of the feeding station, so that we could obtain the first calls produced by the first chickadees to arrive at the food source. We were interested in assessing the chick-a-dee calls produced by the first bird to take seed from a feeding station in 2 contexts. The first context involved calls produced before a second chickadee arrived to take seed from that feeding station. The second context involved calls produced after that second chickadee had arrived to take seed from that feeding station. We hypothesized that a certain note type may serve a recruitment function in chick-a-dee calls, if, on average, relatively greater numbers of that note type were produced by the first bird discovering and exploiting a food source prior to the second bird arriving and taking seed. If a chickadee did not approach within 20 m of the feeding station within 90 min of the observer first setting up, the session was abandoned and the seed was left on the stand.
We recorded 12 different birds between February and April in 3 different years (3 chickadees in 2006, 6 in 2007, 3 in 2008); 11 were color-marked individuals and 1 was unbanded but had distinctive white feathers on its head. This February–April recording window spans the period in which overwintering flocks break up into breeding pairs. Some of our February and early March recordings involved instances of more than one chickadee coming in to the feeding station after the first bird had arrived to take seed, whereas our later March and April recordings involved only one other individual (likely the mate) coming in after the first bird had arrived to take seed. Many other individuals were recorded during our data collection, but only these 12 individuals fit our criteria for inclusion in this study: (1) being individually identifiable, (2) being the first bird to take seed from a feeding station after we stocked it, and (3) producing chick-a-dee calls both before and after a second chickadee arrived at the feeding station to take seed. We recorded calls of birds using Marantz PMD-222 cassette recorders with Maxell XL-II high-bias tape, or Fostex FR-2 digital field recorders (with sample rate of 22 050 and 16-bit resolution), and Sennheiser ME-62 microphones. Observers called out the locations, behavior, and color band markings of birds onto the tape or sound file.
Call analysis
Tapes were digitized using Cool Edit Pro 2.0 (Syntrillium Software) at a sample rate of 22 050 and 16-bit resolution. Note composition of calls was analyzed using the Spectral View window (Blackmann-Harris window function at 256-band resolution) based on published note classifications for Carolina chickadees (Bloomfield et al. 2005). The number of each note type in each call was manually entered into an SPSS spreadsheet. We focused on numbers of notes in these studies because of the earlier suggestion that calls with different note compositions convey different messages to receivers (e.g., Hailman et al. 1985). We scored 3 note categories in the present study (Figure 1). "C notes" are structurally complex notes that generally increase in frequency over the course of the note and span a large frequency range. "D notes" are broadband, with a characteristic harmonic-like structure, and typically have little frequency modulation. "Introductory notes" comprised all the additional note types of Bloomfield et al. (2005) except for their Dh note, which only occurred once in this study, and was included in the D note category.
We determined the number of Introductory, C, and D notes in each call. E.J.M. scored all the recorded calls of the 12 birds for note composition, blind to whether the calls were produced before or after the second chickadee arrived to take a seed. T.M.F. independently scored the notes of each of the calls, and interrater agreement was high (Cohen's kappas: Introductory = 0.930; C = 0.927; and D = 0.977; E.J.M.’s note scoring data went into subsequent analyses). Calls were analyzed for the average numbers per call of these 3 note classes produced by the first bird to take seed both prior to and subsequent to the second bird taking seed, using Wilcoxon signed-ranks tests (SPSS 15.0; SPSS converts the signed-ranks test statistics into Z scores, which are reported below). We adjusted the alpha level to 0.017 in analyses of note composition of calls to correct for 3 comparisons in each test (Introductory, C, D notes), and tests were 2-tailed.
Study 2. Do calls with more D notes recruit receivers to take seed?
Study location
We played back calls to flocks of Carolina chickadees at the University of Tennessee Forest Resources, Research, and Education Center from 5th to 22nd March 2008. Playbacks were carried out at 12 different sites near feeding stations (materials and dimensions of feeding stations described above). Each site was at least 400 m from the closest adjacent site to ensure independence of sites (data from field studies in the winter of 2007–2008 indicate that 58 of 60 [96%] uniquely color-marked birds at 15 different sites separated by this distance were recorded at only one site).
Playback calls
Calls used in the playback study were recorded from 7 different birds (6 were color-marked and 1 was unbanded) in field settings. A Sennheiser ME-66 microphone was mounted atop a microphone stand (1 m high) placed within 1 m of the feeding station to record calls, using a Fostex FR-2 digital field memory recorder with a sample rate of 48 000 and 16-bit resolution. All playback calls were recorded from birds on or within 1 m of a feeding station, when the bird was 0.5–2 m from the microphone.
There were 12 calls used for playbacks, and these were chosen on the basis of quality (primarily, the signaler facing the microphone when it called, and low background noise) and note composition. Because the first study suggested that an increased number of D notes in calls may serve a recruitment function (see below), we used 2 sets of calls that varied in the number of D notes (Figure 1). One set of 6 playback calls had a relatively small number of D notes (range = 2–5). This range of D notes was chosen because it spans the typical number of D notes in calls of this population (an average of 3.4 ± 3.7 SD D notes per call; Freeberg forthcoming). The other set of 6 playback calls had a relatively large number of D notes (range = 7–11). This range of D notes was chosen as it represents roughly twice the number of D notes used in the first playback set and also is in the upper range of D notes produced in the calls of the first birds to exploit seed at a feeding station seen in Study 1 (see below and Figure 2). To try to avoid the possibility of individual differences (such as sex, age, or dominance status) confounding any effect of the number of D notes in calls being played back, 4 of the individuals from which recorded calls were used had both a "few D call" and a "many D call" in the playback sets (birds 3, 4, 6, and 7 in the rows of Figure 1). Each playback call was copied into its own 60-s sound file such that it was repeated once every 10 s, followed by silence (e.g., a 1.1-s duration call would be followed by 8.9 s of silence and that 10-s call-silent interval would be repeated 6 times).
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Playback procedure
A playback speaker (Cambridge Soundworks, Newton, MA) was set on a 2-m stand positioned 2–3 m from, and facing, the feeding station. At the beginning of a playback at a particular site, after the equipment was set up, the feeding station was stocked with roughly 50 g of a 1:1 mix of sunflower and safflower seed. Calls were played back from a laptop PC by the observer sitting behind a camouflage fence blind, 10 m away from the feeding station. The flocks to which, and sites at which, calls were played back did not contain the bird that originally produced the call being played back (as in Freeberg and Lucas 2002
). Only one call exemplar was played back at each site. Each call was played back at 75–76 dB sound pressure level measured at 1 m from the playback speaker using a General Radio (Concord, MA) 1565-B Sound Level Meter with A weighting and fast response. For each site, the 60-s sound file (containing the exemplar for that site played once every 10 s) was played back at the start of each 5-min playback block, followed by 4 min of no playback, and there were 12 5-min playback blocks. At the onset of the first playback block, a digital timer was started. The dependent measure was the latency for a first chickadee to come into the feeding station and take a seed. If no bird took a seed by the end of the 12th playback block (i.e., at 60 min), no more playbacks were conducted, but the timer was run an additional 10 min. Thus, if no bird took a seed at a site, that playback call was given a latency of 70 min. Because of the distributions in the latency data, we tested for an effect of playback call using the 2-tailed Wilcoxon test. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Do birds vary note composition of calls when they detect food?
One hundred and eighty-three calls were obtained from the 12 birds that were the first to arrive and take seed (before the second bird arrived to take seed: average calls/bird = 7.8, range = 2–24; after the second bird arrived to take seed: average calls/bird = 7.4, range = 1–37). More D notes (average numbers per call for each bird) were produced in the calls of the first bird to arrive and exploit food at the feeding station before the second bird arrived, compared with after the second bird arrived (Z = 2.934, N = 12, P = 0.003; Figure 2). For Introductory and C note categories, there were no significant differences between average numbers of notes produced in the calls of the first bird to arrive and exploit food at the feeding station before the second bird arrived, compared with after the second bird arrived (Introductory notes: Z = 0.533, N = 12, P = 0.594; C notes: Z = 0.338, N = 12, P = 0.735; Figure 2). Averaging across the 12 birds, chick-a-dee calls of the first individual to take seed from the feeding station contained a mean of 7.0 total notes (±1.8 standard deviation [SD]) before the second bird arrived to take seed compared with a mean of 4.2 total notes (±1.2 SD) after the second bird arrived to take seed (Z = 3.059, N = 12, P = 0.002).
Do calls with more D notes recruit receivers to take seed?
Carolina chickadees were observed to come within 10 m of the playback speaker and feeding station at 9 of the 12 sites (4 sites with playback calls containing few D notes and 5 sites with playback calls containing many D notes). Carolina chickadees came in and took seed from the feeding stations at 7 of the 12 sites (2 sites with playback calls containing few D notes and 5 sites with playback calls containing many D notes). The latency for birds to take seed was significantly shorter for sites in which the playback calls contained many D notes compared with sites with calls containing few D notes (2-tailed Wilcoxon test; Wx = 26, m = 6, n = 6, P = 0.031; Figure 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Carolina chickadees, like many Parid species, form territorial overwintering flocks of unrelated individuals (Ekman 1989
; Mostrom et al. 2002). Because individuals are often out of visual contact as they move through their territory, vocal signaling serves a fundamental communicative role in these species. One of the most commonly used vocal signaling systems in chickadees is the chick-a-dee call (Smith 1972). To our knowledge, Ficken (1981) was the first to argue explicitly that the call may function in reciprocal altruism within flocks, in that individuals produced chick-a-dee calls when they detected a new food source, and production of these calls could aid in recruiting flockmates to the food source. Our findings indicate that signalers can vary the note composition of their chick-a-dee calls on detecting a food source, producing calls containing more D notes, and this call variation may impact whether and how quickly individuals are recruited to the area. We cannot rule out the possibility that acoustic characteristics of D notes, rather than the number of D notes per se, influenced the behavior of receivers. Acoustic parameters of D notes can change depending on how many D notes occur in a call (Freeberg et al. 2003). Future studies could control this potential confound by artificially constructing playback calls from the same underlying set of D notes that either contained a large or a small number of those notes.
Our results with Carolina chickadees suggest that large numbers of D notes in calls can serve a general communicative function related to recruitment to the location of a signaler. This conclusion contrasts with the results or interpretations of several other studies comparing note composition of chick-a-dee calls to possible functions. For example, Templeton et al. (2005), in a study of black-capped chickadees, suggested that larger numbers of D notes in calls serve a mobbing function in the context of avian predators. Templeton et al. (2005) found that calls with greater numbers of D notes were used in contexts of greater threat (smaller, more agile avian predators) than were calls with fewer numbers of D notes. We note that predator stimuli have been linked to D notes in a recent field study of Carolina chickadees by Nolen and Lucas (forthcoming), to introductory notes in a captive study of black-capped chickadees by Baker and Becker (2002), and to C notes in a field study of Mexican chickadees by Ficken et al. (1994). Whether these differences in findings from these several studies stem from real species (or population) differences, differences in interpretation, or differences in methodology, cannot be resolved at this point. However, we would argue that these differences indicate that the "meaning" of D notes (or, for that matter, any of the note types) is still largely an open question in Parid species.
We did not find that C notes were produced more in calls of birds when they first detected and exploited a food source. This would seem to counter the findings of an earlier study with a different population of this species, which indicated that birds were more likely to take seed from feeding stations when calls were played back containing large numbers of C notes, compared with playbacks without C notes (Freeberg and Lucas 2002). Increased production of C notes in chick-a-dee calls has been associated with flight behavior in Carolina chickadees in 2 different studies (Smith 1972; Freeberg forthcoming). This association between increased usage of C notes in calls and flight behavior offers another interpretation of the earlier findings of Freeberg and Lucas (2002). That playback study suggested that greater numbers of C notes might be associated with food in Carolina chickadees. The design of that experiment was based on a preliminary study of a small number of calls recorded from birds contacting a feeding station for the first time. Flight behavior of the birds producing those calls was not noted, but given the microphone orientation with which those calls were recorded, it is likely that the calls were produced by birds arriving at, on, or departing from, the seed stand. Thus, the "C-rich" calls described in Freeberg and Lucas (2002) may not have been associated with food per se but rather with signaler flight behavior to and from a platform on which birds perch, which happened to contain seed. On the other hand, if this were true, it is less clear why playbacks of calls containing a large number of C notes would be more effective at bringing receivers into a feeding station to take seed, compared with calls containing no C notes and a larger number of D notes. This raises the exciting possibility that the Indiana population of the earlier study and the Tennessee population of this study might be using different note compositions in their chick-a-dee calls to signal food detection. If so, these population differences would indicate geographic variation in note composition (syntax) and call meaning. A direct test of this possibility would be to conduct parallel sets of recordings and playbacks at feeding stations, using the same methodologies, to birds of both populations.
D notes may be the most effective note type at recruiting flockmates to the location of a signaler, in that, like C notes, they are broadband, but unlike C notes, D notes are long in duration and have most of their energy at lower frequencies (Bloomfield et al. 2005). Furthermore, D notes may have greater and more rapid amplitude change at the onset of the note, compared with C notes. All these factors could aid in signaler localizability in medium-range signaling (Wiley and Richards 1982; Bradbury and Vehrencamp 1998). At the level of the call as a whole, a call with many D notes would have a longer duration than a call with few D notes, which could contribute to a higher duty cycle, and may therefore be more effectively detected by a receiver. Receivers—in chickadees, primarily flockmates—may be able to exploit this information gained from the signal and from the signaler's context (Leger 1993; see also discussion of fine-level local enhancement in stable groups by Pöysä 1992).
To conclude, these results indicate that note composition of chick-a-dee calls is associated with the behavior of the signaler in contexts related to detection of food. The first chickadee to arrive at a new food source may experience increased arousal and conflicting motivations to feed or to leave and rejoin the flock. Increased arousal or changes in motivation might influence the note composition of chick-a-dee calls it produced. An individual chickadee experiencing greater arousal, minimal to moderate levels of fear, or tendencies toward aggression might be predicted to produce more D notes, in that they are relatively low-frequency notes that can have a "harsh" acoustic quality to them, according to motivation-structural rules (Morton 1977; Owings and Morton 1998). Receivers, on hearing calls with large numbers of D notes, may be recruited to the area of the signaler, at which time contextual factors (e.g., presence of food or a perched predator) may further influence receiver behavior. The chick-a-dee call offers a strong system for addressing questions of communicative signal structure and function, in that it is a highly flexible signaling system and possesses some of the structural characteristics of human language (Hailman et al. 1985). Our work adds to an understanding of the structural and functional complexities of the chick-a-dee vocal system and points to the need for more intra- and interspecific comparative work.
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ACKNOWLEDGEMENTS |
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Thanks to Richard Evans and the staff of the University of Tennessee Forest Resources, Research, and Education Center. This research was conducted under approved protocol #1248 of the University of Tennessee IACUC. We thank Jessica Owens and Gabriella Lloyd for assistance with data collection during the playback studies and to Jeff Lucas and 2 anonymous reviewers for providing helpful comments on an earlier draft of the manuscript.
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