Contact call diversity in wild orange-fronted parakeet pairs, Aratinga canicularis

ANIMAL BEHAVIOUR, 2006, 71, 1141–1154 doi:10.1016/j.anbehav.2005.09.011

Contact call diversity in wild orange-fronted parakeet pairs, Aratinga canicularis KAT HR YN A. COR TOPA SS I & J AC K W. BRA DBUR Y

Laboratory of Ornithology, Cornell University (Received 17 February 2005; initial acceptance 26 May 2005; final acceptance 28 September 2005; published online 9 March 2006; MS. number: A10096)

Contact calls are used to maintain cohesion and coordinate movements in social animals. The amount and type of identity information provided by contact calls are linked to social organization. Socially stable species often converge on shared group-specific contact calls. In socially fluid species, contact calls tend to be individually distinctive; evidence indicates that such calls are important for mediating individual-specific interactions. Dolphins, for example, will mimic the individually distinctive contact calls of other individuals while socializing. We examined contact calls in another fission–fusion species, the orange-fronted parakeet. Free-living and temporarily captive nonbreeding pairs as well as free-living breeding pairs were recorded. In all contexts, pairs produced multiple (up to nine) discrete contact call types, but like dolphins, typically favoured one to two individually specific variants per bird. The number of dominant variants produced and their evenness of use varied with context. Captive pairs produced the fewest dominants, using them with high evenness. Free-living nonbreeding pairs produced more dominants, and showed similarly high evenness. Breeding pairs varied widely in the number of dominants produced and their evenness of use, showing both the highest and lowest values of each. Latent acoustic measures revealed greater structural variation within and among dominants for free-living compared to captive pairs, presumably reflecting the increased opportunity for social interaction available in the wild. Across contexts, calls could be accurately assigned to pair using acoustic measures; however, within-pair call clustering was not greater than that between pairs. Pairs’ calls were distinctive, but in a way that preserved individual variation. Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Contact calls are important signals mediating interactions among social animals (Marler 2004). This includes establishing new social connections, affirming or re-establishing existing connections, or coordinating movement and spacing among already socializing animals. They are often used when visual contact is unavailable, for example, when visibility is limited by distance or surroundings, or when social crowding makes visual contact with specific individuals difficult. Among their functions, contact calls can locate and assemble members of existing groups, recruit and assemble new members to temporary aggregations, and coordinate group position and movement for foraging, roosting or other shared activities. They range from soft to exceptionally loud sounds, depending on whether socializing animals are close together or far apart. Contact calls often provide information about the identity or social affiliation of the caller. There are many Correspondence: K. A. Cortopassi, Laboratory of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca, NY 14850, U.S.A. (email: [email protected]). 0003–3472/06/$30.00/0

examples of calls providing individual-level (e.g. Earle 1986; Mathevon 1997; Maurello et al. 2000; McComb et al. 2000; Oda 2002) or group-level identity information (e.g. Mammen & Nowicki 1981; Farabaugh et al. 1994; Boughman 1997; Weilgart & Whitehead 1997; Hile & Striedter 2000). Such group-level convergence of contact calls can extend over large geographical areas to form regional dialects (e.g. Wright 1996; Baker 2003). The relative emphasis on individual- versus group-specific contact calls varies with species and context. However, social organization often shapes the amount and type of identity information that contact calls contain (Tyack 1986a, 2000). While long-term call convergence is common in animals with stable social structure, convergence in more fluid societies tends to be short term or absent. Here, animals often show individually distinctive call structure. Such signature calls may be important for mediating individualspecific interactions in these fluid societies (Tyack 2003). Vocal matching, which can have affiliative (Brown & Farabaugh 1997) or agonistic functions (Vehrencamp 2000, 2001), is a common behaviour exploiting call type heterogeneity. If each individual has its own signature

1141 Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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call, short-term matching of another’s signature could be used to gain that individual’s attention and initiate contact (Tyack 1993). Subsequent behaviours would then be specifically directed to a given animal. Vocal signatures may thus be essential for directed communication in highly dynamic fission–fusion societies. Bottlenose dolphins, Tursiops truncatus, appear to fit this model. Dolphins live in fluid fission–fusion societies (Ballance 1990; Connor et al. 2000), and there is considerable evidence that individuals produce distinctive signature calls (McBride & Kritzler 1951; Caldwell & Caldwell 1965; Caldwell et al. 1990; Sayigh et al. 1990, 1999; Smolker et al. 1993; Mann & Smuts 1998; Janik 1999; Tyack 2000, 2003). Highly stereotyped signature whistles account for 70–95% of whistle production in temporarily captive or isolated animals (Caldwell & Caldwell 1965; Tyack 1986a; Caldwell et al. 1990). However, when dolphins interact socially, nonsignature whistle production increases. Long-term captives show increased whistle diversity over time, and nonsignature production occurs most frequently when the entire group is present and interactions are varied (Caldwell et al. 1990; Janik & Slater 1998). In a study of free-ranging dolphins, signature whistles accounted for only 52% of all whistle production (Cook et al. 2004). An exception to such diversity is noted in adult male pairs, one of the few stable associations in this species, where long-term convergence of whistle structure has been reported (Smolker & Pepper 1999; Watwood et al. 2004). Despite the suggestion that signature whistling is an artefact due to the stress of captivity or absence of interacting conspecifics (Tyack 1986b; Caldwell et al. 1990; Janik et al. 1994; McCowan & Reiss 1995; Janik & Slater 1998), recent work comparing individual whistle production across captive and free-living contexts supports the existence of stable signatures (Watwood et al. 2005). Still, observations of socially interacting dolphins suggest that vocal diversity and imitation may be important (Tyack 1986a, 2000). Both captive (Burdin et al. 1975; Gish 1979; Tyack 1986b; Janik & Slater 1998) and free-ranging dolphins (Sayigh et al. 1990; Janik 2000; Tyack 2003) will imitate the signature whistles of other individuals when socializing. These findings suggest that at least some of the increased diversity seen could arise from dolphins mimicking each other’s signature whistles as part of an individual-specific transaction. Wild orange-fronted parakeets, Aratinga canicularis, also live in highly dynamic fission–fusion societies (Bradbury et al. 2001; Bradbury 2003). Like dolphins, temporarily captive parakeets show evidence of individually distinctive contact calls (Cortopassi & Bradbury 2000; Bradbury et al. 2001). Furthermore, wild parakeets will alter their contact calls to partially match the calls of interacting conspecifics or field playbacks (Vehrencamp et al. 2003). These observations suggest that orange-fronted parakeets might use individual signatures and short-term mimicry in a manner similar to that of dolphins. Unfortunately, the data supporting signature calling in this species were collected on captive individuals of unknown social affiliation. Given the social parallels with dolphins, there is a similar concern that production of highly stereotyped

calls could be an artefact of holding wild parakeets in stressful or isolated captive conditions. Free-living parrots may produce so many contact call types that none could function as an individually specific signature. This raises a number of questions. Do orange-fronted parakeets produce signature calls in the wild? If so, is nonsignature call production more likely when social interactions are imminent? Do mated parakeet pairs, like allied male dolphins, show contact call convergence? If both individual signatures and pair convergence are present, how do they play out against each other? To address these questions, we examined the contact call repertoires of wild orange-fronted parakeets from multiple contexts. Repertoires of captive and free-living pairs, from both the breeding and nonbreeding seasons, were assessed and compared. Inherent in each context were differences in the latent opportunities available for social interaction. Because mated pairs are fundamental social units in this species (and the stable elements around which its fluid fission–fusion structure revolves), and because of the difficulty in assigning individual identity to the calls of free-living birds, we focused on pair repertoires. Where individual assignment could be made, those data were also included. Through visual analysis of contact call spectrograms, we assessed the number and relative usage pattern of call variants to determine whether pairs in each context favoured relatively few dominant types (consistent with signature calling) or instead produced a large number of different types. In addition, we measured the structural variation within and among the dominant types encountered to compare mean levels of contact call diversity across contexts, and to determine whether call structure shows convergence within mated pairs in this species.

METHODS

Study Area, Selected Contexts and Bird Recording The study was conducted in the dry forest zone of the Area de Conservacion Guanacaste (ACG), Costa Rica. We observed all policies regarding animal welfare established by the ACG, the University of California San Diego and Cornell University. The breeding season for orangefronted parakeets in Guanacaste runs from mid-December to mid-May, with a peak in activity from February to March. This coincides with the dry season of the Central American Pacific coast. June to November marks the wet season, and is well outside of the normal breeding period for orange-fronted parakeets. Birds recorded during these latter months were almost certainly in nonbreeding condition.

Captive nonbreeding (CNB) pairs In late July and August 1997, two groups of parakeets were held sequentially in an outdoor aviary in the ACG. For group 1, two birds were captured as a pair, and a third was captured a day later at the same location. For group 2, four birds were captured as two pairs on the same day at

CORTOPASSI & BRADBURY: CALL DIVERSITY IN PARAKEETS

a location different from group 1. Prior work on orangefronted captives (Bradbury et al. 2001) focused on individuals of unknown affiliation; here we focused on mated pairs. Using captives allowed us to assign contact calls to specific individuals, and the new focus on pairs reduced the likelihood of atypical calling behaviour. However, it is difficult to capture both pair members, so our eventual sample size was limited. Captives were handled as little as possible (weighed, measured, banded and marked with dye), and held for 1–2 weeks before release into the wild at their capture sites. Pairs were housed with other conspecifics to further reduce captive stress. The aviary (4
2
3 m, built of hardware cloth and wood) contained numerous perches, a rain shelter, and a platform for fresh food and water. Six of the birds immediately displayed signs of pairing characterized by mutual preening, food sharing and close proximity. These are behaviours normally seen in mated pairs in the wild, and many birds netted together do not show them. Parent–fledgling pairs additionally would have shown begging behaviour along with differences in body size and head coloration. Intensive audio–video recordings facilitated the assignment of caller identity to contact call. Only contact calls that could be confidently assigned to an individual, and thus a pair, were used. Although a random subset of these data (240 calls) has been used in a prior analysis (Bradbury et al. 2001), the entire data set for the three pairs (770 calls) has not been presented before, and none of it has been analysed with respect to pair identity or discrete variant class.

Wild nonbreeding (WNB) pairs In June and July 2000, recordings were made of freeliving pairs at various sites around the ACG. We targeted single pairs found at feeding or night roost staging sites. In order to be used, a pair had to have both members calling, not be engaged in any social interactions with other birds, and be close enough to make recording quality comparable to that of the captive and nesting contexts. These stringent requirements again limited the available sample size. In the end, only three pairs fulfilled the conditions and remained long enough to provide at least 20 useable contact call recordings. Because most pairs seen flying together at this time of year are mated, and parent– fledgling pairs are easily distinguishable, we are confident that these were mated pairs. Individual caller identity could not be assigned for any pair.

Wild breeding (WB) pairs In February and March 2000, free-living breeding pairs were recorded at their nest sites. Orange-fronted parakeets build nest cavities exclusively in the arboreal termite mounds of the species Eutermes nigriceps (Hardy 1963). Fifteen active nests were monitored. In this context, pairs could be recorded at the same location on successive days and in the absence of interacting conspecifics. Pair response to encroachment of other parakeets around the nest is rapid and aggressive (K. A. Cortopassi, unpublished observations), and there is no evidence of nest sharing by multiple pairs. However, most breeding pairs are

conspicuously silent around the nest. It took long hours of waiting to obtain the samples presented here. No breeding pairs were held in captivity because of the potential impact on reproduction. Nests were observed in 4- to 6-h blocks from either sunrise to noon (0600–1200 hours), or noon to sunset (1200–1800 hours) (GMT-0600), with observers positioned in concealed locations near the nest tree. Birds were not outwardly disturbed by our presence and maintained normal activity. Only contact calls that could be confidently assigned to a particular breeding pair were used. Positive pair identification was made when birds were observed entering or leaving the nest mound within a recording session. Where possible, individual caller identity was noted. Individual identity could not be tracked over the entire breeding season (because birds were not captured and marked), but in many instances individual identity could be tracked within a recordingobservation bout. Of the 15 pairs monitored, six yielded 20 or more useable contact call recordings. For all three contexts, contact calls were recorded using a directional microphone (Sennheiser model MKH 816 P48), with an open-cell foam windscreen, and either a Hi8 video camcorder (Canon model ES2000) or a digital audiotape (DAT) recorder (HHB Portadat model PDR1000). Microphone power was provided by the DAT recorder or a phantom supply (Stewart Electronics model BPS-1). A tie-clip microphone allowed observer annotation. Calls were digitally acquired using either RTSD version 2.0 (Engineering Design, Belmont, Massachusetts, U.S.A.) or Syrinx sound analysis software (version 2.2b, Burt SyrinxPC, Seattle, Washington, U.S.A.). Calls were output in analogue format, bandpass filtered from 80 to 16 000 Hz (Krohn-Hite model 3550 filter), and then digitally acquired at a 40- or 44.1-kHz sampling rate. Files were saved in RTSD/Signal or WAVE file format.

Measures of Contact Call Diversity Visual assessment Spectrographic analysis was performed in either Signal (version 3.1 or 3.0, Engineering Design) or MATLAB (release 12.1 or 13(SP1), The Mathworks, Natick, Massachusetts, U.S.A.) using a 256-point Hann window, 512point fast Fourier transform (FFT) and 90% window overlap. All calls were free of clutter (e.g. overlapping insects or birds) and had sufficient signal-to-noise ratio (SNR) to provide discernible patterns. The orange-fronted parakeet contact call is a single, harmonically rich note, which can be divided into three consecutive sections based on its time–frequency structure (Cortopassi & Bradbury 2000). Typically, the middle section provides the most striking pattern differences, which relate to the number, position and width of stepwise frequency modulations or harmonic stack insertions (e.g. Fig. 2b at 150 ms, Fig. 4a at 100 ms for examples of the latter). All calls from a particular pair were considered as an ensemble and sorted into discrete variant classes without regard to caller identity. This was done for all pairs because for most contexts, individual bird identity could not be assigned. Calls were sorted based on overall differences in

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acoustic structure. As with the songs of many passerines, call types were sufficiently discrete within a pair to permit straightforward grouping by eye. We determined which of the variant types were observed with a frequency greater than 5%; these were termed dominant variants. Following the ecological literature (Hill 1973), we term the total number of dominant variants the richness, S, of a pair’s dominant contact call repertoire. As an overall diversity measure, X we computed the Shannon–Wiener index, S H¼ i¼1 pi log2 pi , where pi is the proportion of dominant type i among the S dominants. From this, we calculated the relative diversity, or evenness of the dominant repertoire, E ¼ H/Hmax, where Hmax ¼ log2(S ). Evenness ranges from zero to one, achieving its maximum when all S dominants are used equally. Differences in overall diversity H between pairs can thus be partitioned into differences in richness S and evenness E. Overall diversity is largest when S is large and E is close to one, and smallest when S is small and E is close to zero. Plots of S and E helped to identify sources of convergence or divergence in H values among pairs. Finally, overall diversity was used to back-calculate an equivalent richness value S0 ¼ 2H. S0 equals the number of dominant variants that, if evenly used, would give a pair diversity value equal to the observed H. Equivalent richness transforms overall diversity into the same units as richness. S0  S, and the smaller the value of E, the smaller S0 will be relative to S. Both S and S0 values can be divided by two to give average per bird estimates of richness and equivalent richness.

Cross-correlation and ordination Spectrographic cross-correlation (Clark et al. 1987) and ordination by principal coordinates (Gower 1966, 1987; Legendre & Legendre 1998), or SPCC-PCO analysis (Cortopassi & Bradbury 2000), was used to assess the structural variation within and among the discrete dominant classes identified in the visual analysis. We obtained a call sample, stratified across dominants, for each focal pair. Sounds were up-sampled to 44.1 kHz and power spectrograms (in dB) were generated in MATLAB using the previous settings. Correlation techniques are robust against random background noise (e.g. wind or leave rustle), and only clutter-free, adequate SNR calls were used. However, additional steps were taken to reduce spurious background. Spectrograms were band-limited from 500 to 10 000 Hz, and a median-based background noise reduction scheme was applied. The method involved thresholding to zero all values in the spectrogram smaller than the median power value (presupposing that these spectrogram bins contained noise elements only), and was effective in eliminating broadband background noise. To validate the method’s effectiveness, we calculated a proxy for signalto-noise ratio as root-mean-square (RMS) amplitude of the signal bins over RMS amplitude of the noise bins for each call prior to denoising. Mean call SNR and SNR absolute deviation from the mean were compared to mean call spread in PCO space (using natural log or square-root transformation, where needed, to normalize). Both SNR and SNR deviation were uncorrelated with call spread

(see Results). Thus, we believe that the variation observed reflects true structural differences. Spectrogram preprocessing and cross-correlation in time were performed using a custom MATLAB routine (from K.A.C.), and all pairwise peak correlation values were returned. Principal coordinates analysis of the peak correlation matrix produced an ordering for the calls in PCO space (Cortopassi & Bradbury 2000). The PCO axes constitute latent orthogonal acoustic measures for the dominant call sample. We used the PCO measures to assess: (1) the overall structural variation of the pairs’ dominant repertoires; (2) whether pairs were identifiable based on dominant call structure; and (3) whether there was any convergence of dominant calls within pairs. These analyses rely only on the assumption that a representative number of calls were recorded from each pair member, and not on individual identification per se. Representative coverage was certain for CNB pairs. While only some individual assignment was possible for wild pairs, both pair members were observed to call during recording bouts of all WNB pairs, and most or all WB pairs. Furthermore, the total number of dominants observed for each WB pair was always greater than the number of dominants observed for any one pair member in identified calling bouts. By stratifying our random sample across all dominant classes (rather than drawing from the pooled sample for a pair), we avoided overrepresenting any one frequently used dominant and thus any one relatively vocal mate. We used Euclidean distance between each dominant call in the random sample and its group centroid in PCO space as our measure of structural variation. Euclidean distance was used rather than a statistical or Mahalanobis distance because the latter corrects for variation differences and would defeat our objective of actually quantifying variation differences between dominants in the same space. Distances were calculated using the first five PCO axes, which captured 85% of the full ordination. Centroid distance values were log-transformed (natural log) to correct for deviations from normality and used in an analysis of variance (ANOVA) to assess whether pairs varied significantly in levels of structural variation within and among dominants. Larger mean centroid distances represent greater levels of variation within a given set of calls. Values are reported as mean  standard error. Degrees of freedom were adjusted down appropriately based on the number of group centroids estimated. Pairwise comparisons were made using a Tukey–Kramer honestly significant difference (HSD) test with alpha level of 0.01 or 0.05. Finally, PCO measures 1–5 were used in both a multivariate analysis of variance (MANOVA)/linear discriminant function analysis (LDA) and in a Ward’s hierarchical cluster analysis. MANOVA/LDA determined whether between-pair means were sufficiently different that calls could be correctly assigned to pair based on their latent acoustic measures. Cluster analysis determined whether within-pair calls showed greater clustering than betweenpair calls in multivariate space. Statistical tests were performed using either JMP (version 4.0.4, SAS Institute, Cary, North Carolina, U.S.A.), or SPSS (version 8.0.0 SPSS, Chicago, Illinois, U.S.A.).

CORTOPASSI & BRADBURY: CALL DIVERSITY IN PARAKEETS

RESULTS

(a)

CNB

WNB

WB

Table 1. Summary of results from visual analysis of call spectrograms for all focal pairs

Context CNB CNB CNB WNB WNB WNB WB WB WB WB WB WB

Pair ID

N

Variant total

WT XR YP D2.10 D5.34 D6.36 SRP026 SRP004 SRP013 SRP010 JEN011 PAN003

306 256 208 20 31 49 53 51 165 43 32 182

6 6 7 4 4 5 5 7 8 3 5 9

Dominant use (%) 47, 52, 48, 50, 48, 55, 51, 75, 76, 84, 53, 31, 15,

46 44 46 35, 10 26, 23 24, 16 40 8, 6 14, 5 9, 7 31, 6, 6 20, 18, 10

Pooled dominant use (%) 94 96 94 95 97 96 91 88 95 100 97 95

Variant total: total number of call types produced by a pair; dominant use: fraction (percentage) of the pair’s call total accounted for by each dominant type; pooled dominant use: fraction (percentage) of the pair’s call total accounted for by all dominants.

2

1

0

4

4

2

2

0

0

Equivalent richness

Richness

(b)

(c)

Evenness

1

0.5

026 SRP 004 SRP 013 SRP 010 JEN 011 PAN 003

SRP

D2.

10 D5. 34 D6. 36

0 WT XR YP

Table 1 summarizes the number of calls analysed, total number of variants detected, and relative use of dominant variants for each focal pair in each context. Figure 1 shows the overall diversity, richness, equivalent richness and evenness of each pair’s dominant repertoire. Pairs produced three to nine total contact call variants, and the number of dominant variants (richness) ranged from two to five. There was a just-significant relationship between sample size and total number of variants observed (linear regression: R2 ¼ 0.33, t10 ¼ 2.20, P ¼ 0.053), but no relationship between sample size and total number of dominant variants observed (linear regression: R2 ¼ 0.096, t10 ¼ 1.03, P ¼ 0.33). Thus, we believe that we identified all dominant call types used by each of the 12 focal pairs. The three captive pairs showed low diversity values, with low richness but high evenness. Each CNB pair produced two dominant call types out of the six to seven total variants available per pair. Dominants were used evenly, so equivalent richness equalled richness in all pairs. Call identity was known in this context, so we observed that each captive bird had its own signature dominant, which it used 89–97% of the time. Figure 2 shows an exemplar for each individual’s dominant call. In no case did pair members share dominant variants with each other, or with any other bird in their aviary group. Matching of a pairmate’s dominant occurred but was rare, ranging from only one to three calls (0.6–2.6%) out of all those produced by an individual. The three wild nonbreeding pairs showed higher diversity values than the captive pairs, resulting from higher richness and comparable (or slightly lower) evenness. Each WNB pair produced three dominant call types out of the four to five total variants available per pair. All pairs

Diversity

Diversity Based on Visual Classification

Pair ID Figure 1. (a) Shannon–Wiener diversity, H, (b) richness, S (closed symbols) and equivalent richness, S0 (open symbols) and (c) evenness, E, values for the dominant repertoires of all focal pairs. CNB: captive nonbreeding pairs; WNB: wild nonbreeding pairs; WB: wild breeding pairs. WB pairs are ordered by breeding stage, with earlier stages to the left.

shared a similar pattern of dominant usage, with a single variant comprising half or more of a pair’s dominant utterances. Because of this skewed usage pattern, equivalent richness was slightly lower than richness for all WNB pairs. The six wild breeding pairs displayed remarkable variation in all usage indexes, showing both the highest and lowest values of overall call diversity, and a striking range of dominant richness and evenness values. The WB pairs produced from two to five dominant call types out of the three to nine total variants available per pair. Figure 3 shows the distributions of all variants identified for three WB pairs that span the range of diversity, richness and evenness seen. The SRP026 pair (Fig. 3a) showed two evenly used dominant variants, giving a level of diversity comparable to that of the captive pairs. In contrast, the SRP004, SRP013 (Fig. 3b) and SRP010 pairs each showed three dominant variants with one used markedly more

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10 Frequency (kHz)

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2

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2 0

100

200

0

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Time (ms) Figure 2. Exemplars of dominant contact call types for captive nonbreeding individuals (a) W, (b) T, (c) X, (d) R, (e) Y and (f) P.

than all the others. Although richness was higher for these pairs, the low evenness resulted in low overall diversity, and thus equivalent richness was much less than richness. Finally, the JEN011 and PAN003 (Fig. 3c) pairs each showed a high number of dominant variants. The JEN011 pair used two of its four dominant variants markedly more than the others. The high richness but low evenness resulted in overall diversity and equivalent richness values comparable to those of the WNB pairs. The PAN003 pair used its five dominants evenly, and equivalent richness was comparable to richness. Both the high richness and high evenness seen in this pair resulted in high overall diversity, the highest value observed for all the focal pairs. Stages of breeding for the WB pairs were roughly estimated from their patterns of nest visits or from detection of chick calls within the nest mounds. Based on this, the SRP026 and SRP004 pairs were either near the end of incubation or with younger nestlings (early), the SRP013 pair appeared to have younger nestlings (middle), and the SRP010, JEN011 and PAN003 pairs all had older vocal nestlings (late). While there were insufficient samples for statistical testing, the results suggest a tendency towards increasing dominant richness and overall diversity as the stage of nesting progresses (Fig. 1). When possible, WB individuals were tracked within an observation bout, and calls were assigned to one or the

other bird of the pair. Thirteen bouts allowed identification of five or more calls. The patterns of calling in these identified bouts matched the overall patterns of calling seen in pooled observations for pairs (Fig. 3). Single birds produced one to many distinctive contact call variants, and the majority of these variants were identified among the dominants for the pair (Fig. 4). As with the CNB pairs, we observed no sharing of dominant variants by WB pair members. In fact, in all bouts where both birds were calling, we observed no variant sharing of any kind. The calling diversity (richness and equivalent richness) calculated for individual birds in these bouts was equivalent to or greater than that estimated from pair averages. For example, in a bout with both SRP013 pair members calling, per-bird equivalent richness values were 1.8 and 1.0. Both values are higher than the average per-bird equivalent richness of 0.94 calculated for the pair considered together. This bout and the pooled data (Fig. 3b) suggest that one pair member produced two of the three dominant types (Fig. 4c, d) and did most of the calling at the nest. It was the relative silence of one pair member that diminished overall pair diversity. In three combined bouts with the same (putatively) PAN003 bird calling, per-bird equivalent richness was 2.9. This value is higher than the average per-bird equivalent richness value of 2.3, and much higher than any equivalent richness value obtained for any other pair or individual in any context.

CORTOPASSI & BRADBURY: CALL DIVERSITY IN PARAKEETS

(a) 0.6

0.4

0.2

(b) 0.8

Frequency

0.6

0.4

0.2

(c) 0.4

0.2

1

3

5

7

9

Variant number Figure 3. Frequency distributions of all variants identified for wild breeding pairs (a) SRP026, (b) SRP013 and (c) PAN003.

Diversity Based on SPCC-PCO Analysis The stratified sampling scheme yielded up to 40 dominant calls per pair. In all, 440 calls from the 12 focal pairs were analysed using SPCC-PCO. Figure 5 shows ordination of the dominant call sample in PCO axes 1 and 2, which together accounted for 70% of the original intercall distances. While the ordination was calculated for all 440 calls taken together, each pair is plotted separately to allow better visualization of the pair’s dominant sample. We observed that the WNB and WB birds tended to show greater overall dominant call spreads (and thus structural variation) than the CNB birds. To test this statistically, five-dimensional centroid distances were calculated from each dominant centroid (for

all calls from each dominant type), and from each pair centroid (for all calls from each pair). This allowed us to determine whether the levels of structural variation within discrete dominant types, and among all dominant types used by a pair, varied across contexts. PCO axes 1–5 accounted for 85% of the original intercall distances. There was no relationship between group sample size and mean dominant-based (linear regression: R2 ¼ 0.00052, t33 ¼ 0.13, P ¼ 0.90) or pair-based (linear regression: R2 ¼ 0.012, t10 ¼ 0.35, P ¼ 0.74) centroid distance. Furthermore, there was no relationship between mean call SNR and mean dominant-based (linear regression: R2 ¼ 0.0054, t33 ¼ 0.42, P ¼ 0.68) or pair-based (linear regression: R2 ¼ 0.048, t10 ¼ 0.71, P ¼ 0.50) centroid distance. There was also no relationship between mean call SNR deviation and mean dominant-based (linear regression: R2 ¼ 0.058, t33 ¼ 1.42, P ¼ 0.16) or pair-based (linear regression: R2 ¼ 0.23, t10 ¼ 1.71, P ¼ 0.12) centroid distance. Thus, we conclude that our analysis captured legitimate variation differences. Distance measures were grouped by context (CNB, WNB or WB) and an ANOVA was performed. There were significant differences between the three contexts for both dominant-based (ANOVA: F2, 402 ¼ 12.72, P < 0.0001) and pair-based (ANOVA: F2, 425 ¼ 56.60, P < 0.0001) centroid distance means. In both cases, WNB and WB birds showed higher means than did CNB birds (X  SE untransformed centroid distance means: dominant-based: CNB: 0.085  0.0034, N ¼ 120; WNB: 0.099  0.0043, N ¼ 89; WB: 0.12  0.0049, N ¼ 231; pair-based: CNB: 0.099  0.035, N ¼ 120; WNB: 0.20  0.0093, N ¼ 89; WB: 0.17  0.0062, N ¼ 231). Pairwise comparisons between contexts using Tukey HSD revealed significantly different means (a ¼ 0.01) for the WB birds compared to the CNB birds for both dominant-based and pair-based centroid distance. WNB birds fell between the CNB and WB group means for dominant-based distance, and showed close to but not significant differences from either. All contexts were significantly different from one another for pairbased distance, with WNB birds showing the highest mean. Figure 6 shows a plot of dominant-based and pair-based centroid distance, ANOVA means and confidence intervals for the three contexts. When distance measures were grouped by pair, contrasts using Tukey HSD revealed that three of the WB pairs (JEN011, SRP013, SRP026) showed significantly greater dominant-based means (a ¼ 0.05) than did two of the CNB pairs (WT, XR), and a fourth WB pair (PAN003) showed a significant difference from one of the CNB pairs (WT). The remaining two WB pairs (SRP004, SRP010) were not significantly different from the CNB or WNB pairs. These two WB pairs had the lowest values of Shannon– Wiener diversity seen among the 12 focal pairs. Thus, when overall discrete diversity was low, within-dominant structural diversity seemed to drop as well. When pairbased distances were examined, contrasts revealed that five of the WB pairs (JEN011, SRP013, SRP026, PAN003, SRP004) and all three of the WNB pairs showed significantly higher means (a ¼ 0.05) than did two of the CNB pairs (WT, XR), and two of the WB pairs (JEN011, SRP013) and one of the WNB pairs (D6.36) were significantly

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(f)

(g)

(h)

10 6 2

Frequency (kHz)

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10 6 2

10 6 2 0

100

200

0

100

200

0

100

200

Time (ms) Figure 4. Exemplars of dominant contact call types for individuals (assigned during identified calling bouts) in wild breeding pairs. Pair SRP026: (a) type 1, only dominant used by one pair member; (b) type 2, only dominant used by the other pair member. Pair SRP013: (c) type 1, principal dominant used by one pair member; (d) type 2, secondary dominant used by the same pair member; (e) type 3, only dominant used by the other pair member. Pair PAN003: (f) type 4; (g) type 5; (h) type 6, three dominants used by presumably one pair member.

different from all three CNB pairs. The remaining WB pair (SRP010) was not significantly different from the CNB pairs. Thus, there was a clear statistical trend towards the greatest structural variation, both within and among dominants, for the WNB and WB pairs. In addition, other factors within the WB context appeared to be modulating this structural variation. Lastly, we looked for evidence of within-pair call convergence. No overt matching of discrete dominant types was observed between pairmates in the visual analysis. However, this does not preclude some other quantifiable convergence of contact call structure, and the possibility that pair affiliation information is readily available in acoustic measure space. Call convergence could occur in at least two ways: (1) the calls of a pair could converge by clustering tightly in call-measure space (here within-pair calls would be closer to each other than to between-pair calls); (2) the calls of a pair could partition into a distinct region of call-measure space while not concurrently clustering tightly (here within-pair calls would not be closer to each other than to neighbouring between-pair calls). In both cases partitioning would occur, but in only the first case would clustering occur. Thus, our analysis was two part: (1) we used MANOVA-LDA to determine whether pairs’ dominant calls tended to partition into distinct regions of PCO space; (2) we used Ward’s hierarchical cluster analysis to determine whether pairs’ dominant calls tended to ordinate in closer physical proximity in PCO space.

MANOVA using pair identity as a factor revealed significant differences between the 12 focal pairs (MANOVA: Wilks’ l ¼ 0.025, F44, 1627 ¼ 59.65, P < 0.0001). LDA correctly classified 68% of the calls to pair (66% using bootstrapping cross-validation). Table 2 shows the assignment of predicted and actual pair identity for the LDA. Eight of the 12 pairs showed 63% or higher correct call classification. Although assignment faltered for the D2.10, D5.34, SRP013 and JEN011 pairs, where only 26%, 50%, 23% and 35% of the calls, respectively, were correctly classified, sufficient call parameters were shared in five-dimensional PCO space to discriminate pair identity with reasonable accuracy most of the time. Cluster analysis, however, did not reveal a consistent trend towards increased within-pair call proximity. Since we were investigating the spatial proximity of 12 pairs, the first 12 clusters identified were examined. Clusters did not show a strong correspondence with pair identity. Five of the 12 pairs had 68% or more of their calls assigned to a common cluster; these included the three CNB pairs and the WNB pairs SRP004 and SRP010 (the same pairs showing the lowest structural variation in the centroid distance analyses). For the remaining seven pairs, calls were split among two or more different clusters. Table 3 shows cluster assignments broken down by pair. Thus, while calls of pair members tended to occupy the same region of PCO space, they did not tend to show tight clustering with each other overall.

CORTOPASSI & BRADBURY: CALL DIVERSITY IN PARAKEETS

(a)

(d)

(g)

(j)

(b)

(e)

(h)

(k)

(c)

(f)

(i)

(l)

0.3 0 −0.3

PCO 2

0.3 0 −0.3

0.3 0 −0.3 −0.3

0

0.3

−0.3

0

0.3

−0.3

0

0.3

−0.3

0

0.3

PCO 1 Figure 5. Plots of principal coordinate (PCO) 2 versus PCO 1 for the dominant call samples from pairs in each context. Captive nonbreeding pairs: (a) WT; (b) XR; (c) YP. Wild nonbreeding pairs: (d) D2.10; (e) D5.34; (f) D6.36. Wild breeding pairs: (g) SRP026; (h) SRP004; (i) SRP013; (j) SRP010; (k) JEN011; (l) PAN003.

As mentioned in the Methods, a potential concern here is that asymmetric sampling may have occurred when individual identity was unknown. An oversampled individual might artificially reduce variability and inflate within-pair classification success and clustering. Because of our recording criteria and sample stratification, we do not believe that this was the case. However, the pairs that consistently showed the lowest variability (with both high classification success and call clustering) were the CNB pairs, the only pairs with complete identity information and unequivocally equal representation. This result is opposite of that predicted above. Furthermore, we found no significant differences between contexts in either classification success (percentage of calls (arcsine transformed) correctly classified: ANOVA: F2,9 ¼ 0.36, P ¼ 0.71) or clustering (largest percentage of calls (arcsine transformed) assigned to one cluster: ANOVA: F2, 9 ¼ 1.63, P ¼ 0.25). DISCUSSION

Contact Call Use and Diversity One goal of this study was to determine whether wild orange-fronted parakeets produce individually distinctive signature calls. Focal pairs produced a total of three to nine visually distinctive contact call types, two to five of which were dominant for a pair. These dominants accounted for 88–100% of a pair’s total recorded contact

calls. This gave an estimated value of 1–2.5 dominant call types per bird, with a mean  SE of 1.46  0.13, for the 24 birds (12 focal pairs) examined. Diversity values, which incorporate both the richness and evenness of a pair’s dominant repertoire, were 0.78–2.2, corresponding to a mean  SE of 1.20  0.12 equivalent dominant call types per bird. Based on identified calls for CNB and WB pairs, pairmates did not appear to share dominant variants. Thus, parakeets in our study consistently relied on only a few of the total contact call types available to them, and they used these with enough frequency and exclusivity to be consistent with signature types. In addition, call variation appeared to be context dependent, both in the number and usage of discrete dominant types, and in the continuous structural variation within and among those types. While captive pairs showed two dominant call types per pair, and free-living nonbreeding pairs showed three, free-living breeding pairs showed two to five dominant call types per pair (X  SE ¼ 3:33  0:42). Each CNB and WNB pair used its dominants 94% or more of the time, with high evenness. Each WB pair used its dominants 88% or more of the time, and although most breeding pairs showed more dominants than did captive pairs, they varied widely in their evenness of use. While some WB pairs showed highly skewed patterns of dominant usage, others selected among them evenly. As a result, equivalent richness values were both higher and lower than those seen in either the CNB or WNB pairs, with a mean  SE of 2.47  0.47 per pair.

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ANIMAL BEHAVIOUR, 71, 5

space to explore two alternative mechanisms of convergence: the first involves clustering, so that calls within a pair are closer to each other than to calls from other pairs; the second involves partitioning, so that calls within a pair are adjacent but not necessarily closer to each other than to calls from other pairs. Results from MANOVA-LDA and cluster analysis support partitioning but not clustering. For a majority of pairs, calls sorted into their own distinct region of PCO space with a high level of significance, and LDA based on these PCO measures classified calls to pair with reasonable accuracy. Despite their differential use of PCO space, pairs’ calls did not show an overall tendency to be closer to each other than to nearby, nonpair calls. For the majority of pairs, cluster analysis based on the same PCO measures tended to split pair calls between clusters rather than join them. Often, this factor contributed to large within-pair call spreads. In addition, for all pairs where individual identification was made, we observed no sharing of dominant call variants between pairmates or obvious call matching.

(a)

−1

−2

−3

Log centroid distance

1150

−4

(b)

−1

Comparison with Other Species and Interpretations −2

−3

CNB

WNB

WB

Context Figure 6. Dominant-based (a) and pair-based (b) log centroid distance versus context. The horizontal line shows overall centroid distance mean, diamonds show within-level means and confidence intervals. Circles show significance in simultaneous contrasts of all contexts, with nonoverlapping circles indicating significant difference. CNB: captive nonbreeding pairs; WNB: wild nonbreeding pairs; WB: wild breeding pairs.

Ordination using SPCC-PCO analysis revealed low call spreads for CNB pairs, and higher spreads for both WNB and WB pairs. Analysis of dominant-based and pair-based centroid distance revealed that the greater spreads were attributable to both greater within-dominant structural variation (large spreads within a pair’s dominant types) and greater within-pair structural variation (large spreads among a pair’s dominant types). Thus, the free-living orange-fronted parakeet pairs in our study tended to show both greater discrete and continuous contact call variation than did those pairs that were held briefly in captivity.

Convergence of Pair Calls Another goal was to determine whether a pair’s dominant contact call repertoire showed structural convergence. We examined ordination of pairs’ calls in PCO

Like dolphins, the wild orange-fronted parakeets in our study relied on a small number of individually specific contact call types for most occasions. Our birds also used only a subset from the much larger set of call types that they were capable of producing. This finding supports the notion that orange-fronted parakeet contact calls, like dolphin whistles, can function as individual signatures. Signature contact calls have been described previously in domesticated budgerigars, Melopsitacus undulatus (Farabaugh et al. 1994) and captive spectacled parrotlets, Forpus conspicillatus (Wanker et al. 1998; Wanker & Fischer 2001). Our results complement these studies, providing evidence that such signatures also occur in the wild. Long-term convergence of contact calls is often seen when animals form stable social affiliations. The mated pair is the only long-term association observed in wild orange-fronted parakeets (Bradbury et al. 2001). While we cannot fully exclude sharing in free-living pairs due to limited identity information, based on CNB and identified WB birds, we found no evidence of within-pair contact call sharing or call convergence through clustering, both of which have been reported in dolphins (Tyack 1986b; Smolker & Pepper 1999; Watwood et al. 2004) and domesticated budgerigars (Farabaugh et al. 1994; Bartlett & Slater 1999; Hile & Striedter 2000; Hile et al. 2000). We did, however, find evidence of convergence through partitioning. Pairs’ calls tended to occupy the same region of PCO space, but most were no closer to each other than to neighbouring nonpair calls. Even for the few pairs that did show clustering, dominant variants were not obviously similar (Fig. 2) and they were easily assigned to individual. Taken together, these results suggest that there are strong but opposing forces favouring contact calls that provide both individual and pair identity information in orange-fronted parakeets. Given that parakeets must

CORTOPASSI & BRADBURY: CALL DIVERSITY IN PARAKEETS

Table 2. LDA classification of pair identity (using PCO 1–5) for 440 calls from the 12 focal pairs Predicted pair ID Actual pair ID

WT

XR

YP

D2.10

D5.34

D6.36

SRP026

SRP004

SRP013

SRP010

JEN011

PAN003

WT XR YP D2.10 D5.34 D6.36 SRP026 SRP004 SRP013 SRP010 JEN011 PAN003

28 0 5 3 1 0 0 0 3 0 5 8

0 39 2 0 0 0 0 0 0 0 0 0

0 1 27 5 4 0 1 0 1 0 2 0

6 0 6 5 5 0 0 0 2 0 0 0

0 0 0 4 15 0 4 2 3 0 1 2

0 0 0 0 0 40 0 0 0 0 0 0

0 0 0 0 0 0 30 4 4 0 3 0

0 0 0 0 3 0 2 31 7 0 1 1

0 0 0 1 1 0 1 1 9 0 3 1

0 0 0 0 0 0 0 0 1 37 2 3

0 0 0 0 0 0 2 1 5 0 11 0

6 0 0 1 1 0 0 1 5 3 3 25

Values are the number of calls assigned to a particular pair classification.

encode any identity information within a fairly structured, species-specific call template (Cortopassi & Bradbury 2000; Bradbury et al. 2001; J. W. Bradbury, unpublished observations, on recordings from throughout species’ range), there is a likely trade-off between the fraction of variation available for coding individual identity and the remainder available for coding pair identity. A convergence mechanism that involves clustering of a pair’s calls in acoustic space (with gaps between neighbouring pair clusters) necessarily limits the variation available for coding individual identity. This mechanism, while providing for good discrimination among pairs, may make discrimination between individuals of the same pair more difficult. An alternate mechanism that involves spatial partitioning only (and no additional clustering) frees up more of the available variation for coding individual identity. Pushing too far in the direction of separating individuals, however, could result in large within-pair call spreads and make pair identification more challenging. While individual and pair discrimination abilities have not yet been examined in wild orange-fronted parakeets, the results presented here suggest that individual

identification may be more important in this species than pair identification per se. Free-living parakeets in our study typically produced more dominant call types than captive birds. With only one exception, dominant richness in WNB and WB pairs exceeded that of CNB pairs. In addition, free-living birds showed greater continuous structural variation than captive birds when dominants were examined in PCO space. This greater variation was seen both within and among the dominant types produced by a pair. Related observations have been made for bottlenose dolphins, where whistle repertoires obtained from socially isolated individuals are seen to be more limited in number and more highly stereotyped than those obtained from animals in varied social contexts (Caldwell et al. 1990; Janik & Slater 1998). In these parrots, as in dolphins, normal social life in the wild involves frequent fission and fusion of social units. There is growing evidence in both taxa that contact calls are important in mediating these events (Janik 2000; Bradbury 2003; Tyack 2003; Vehrencamp et al. 2003). Interactive playback studies suggest that wild orange-fronted

Table 3. Wards cluster assignment (using PCO 1–5) versus pair identity for 440 calls from the 12 focal pairs Cluster Pair ID

1

2

3

4

5

6

7

8

9

10

11

12

WT XR YP D2.10 D5.34 D6.36 SRP026 SRP004 SRP013 SRP010 JEN011 PAN003

27 0 5 5 4 0 0 2 3 0 1 19

0 0 0 0 0 20 0 0 0 0 0 0

9 0 1 0 0 0 1 0 14 1 8 13

0 0 0 0 0 20 0 0 0 0 0 0

0 0 0 0 0 0 12 4 4 0 14 0

0 39 1 0 1 0 0 0 0 0 0 0

4 1 33 10 18 0 3 0 0 0 3 0

0 0 0 3 3 0 4 33 11 0 1 1

0 0 0 0 0 0 0 0 3 0 3 0

0 0 0 0 0 0 20 0 1 0 0 0

0 0 0 1 4 0 0 1 3 0 1 2

0 0 0 0 0 0 0 0 1 39 0 5

Values are the number of calls assigned to a particular cluster.

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parakeets may temporarily modify their individual contact calls to partially match the signature calls of birds in nearby groups (Vehrencamp et al. 2003). Copying of other group members’ contact calls has also been described in free-living dolphins, and may be a mechanism for mediating social dynamics in this species (Janik 1999, 2000; Tyack 2000, 2003). A logical consequence of such matching or attempted matching, is an increase in the amount of call variation displayed by individuals. Wild-caught captives of each taxon are unable to leave their current social groups or join others, so they may have no need for the degree of contact call variation seen in more socially dynamic contexts. Individual signature calling may begin to dominate. Such individual signatures can be seen as a necessary condition for the facultative matching done by animals interested in directing actions towards a particular individual. This could explain why the preservation of individual identity information is sufficiently important that it constrains structural convergence within orange-fronted parakeet pairs. Both dolphins and orange-fronted parakeets are able to produce a number of different contact call variants in addition to their dominant variants, an ability that is seen in budgerigars as well (Farabaugh et al. 1994). Perhaps this capacity is necessary both for short-term mimicry, which has been observed in dynamic social exchanges of orangefronted parakeets (Vehrencamp et al. 2003) and dolphins (Janik 1999, 2000; Tyack 2000, 2003), and for longer-term mimicry, which has been observed during formation of social alliances in bugerigars (Farabaugh et al. 1994; Bartlett & Slater 1999; Hile et al. 2000) and dolphins (Tyack 1986b; Smolker & Pepper 1999; Watwood et al. 2004). Wanker et al. (2005) suggested that captive spectacled parrotlets use referential signals to address their social companions. Birds name their groupmates with particular contact call labels. In return, named birds respond preferentially to the use of their label by that caller. Such a process could result in high levels of contact call variation without invoking matching of self-advertised signature calls. This process, however, implies significant group stability. Recipients of the naming process would require prior experience in order to recognize the labels conferred on them. Given the fluid composition of orange-fronted parakeet groups, mimicry of another bird’s signature call, rather than use of externally applied labels, seems a more likely explanation for our results. More work is needed to evaluate these interesting alternatives. A main goal of this study was to quantify contact call diversity in orange-fronted parakeet pairs when they were not socializing with other pairs. Socializing parakeets may mimic each other’s calls, so we saw this as the best way to determine whether birds of this species typically use a limited enough number of call types that they could act as individual signatures. While the answer is yes, we still observed that free-living pairs tended to produce more discrete dominant types, with more structural variation within and among those types, than did captive birds. A possible explanation may arise from the simple fact that free-living parakeets are never truly isolated. In captivity, our birds had limited opportunity for natural social interaction with other pairs or flocks. In contrast, wild

solitary pairs in the nonbreeding season are rare; most pairs are observed as part of foraging or roosting flocks, and fission–fusion events within and among groups are common. In the wild, pairs may be constantly seeking or promoting opportunities for social exchange with other pairs or flocks. Thus, while the nonbreeding pairs we recorded in the wild appeared to be isolated, it is entirely possible that the calls they produced were efforts to establish or re-establish contact with other birds in the vicinity. Their calling was intended to be interactive as far as the birds were concerned, and therefore included multiple call types. A similar logic may be applied to the breeding pairs. Breeding pairs are highly aggressive around their nest sites, and social interactions with other pairs, rather than sought out, are actively opposed (K. A. Cortopassi, unpublished observations). It is consistent then, that one of the pairs recorded at the earliest stage of breeding showed low repertoire diversity similar to that of the captive birds. As chicks hatch, however, new opportunities for social interactions arise. Breeding pairs outside the nest frequently exchange contact calls with their chicks inside the nest (K. A. Cortopassi, unpublished observations). Because the four to five eggs in parakeet nests hatch asynchronously, as with most parrots (Forshaw 1989), the number of nestlings that could exchange contact calls with their parents increases over the breeding cycle. This may explain why the dominant richness of adult breeding pairs appeared to increase with nest stage. Whether or not the increased contact call diversity was due to parental mimicry of nestling calls remains to be seen. In addition, the foraging demands on parents provisioning their chicks must certainly increase as the nesting cycle progresses. It may be the case that late-stage pairs seek to join other groups in order to increase their foraging success. If so, such pairs might broadcast more contact call variants than early-stage pairs, who can forage well enough on their own. A consistent interpretation for all of these results is that those contexts showing higher levels of contact call diversity were those for which social interactions were more likely and desirable. Acknowledgments We thank Roger Blanco Segura of the ACG for his support throughout the project and help in obtaining permits, Hugo Guadamuz Rojas for his expertise in locating breeding sites, Anik Clemons and Meade Krosby for field assistance in the spring of 2000, Amy Kelsey, Rodd Kelsey and Marissa Azzara for field assistance in the summer of 1997, Meade Krosby and Amy Therrell for laboratory assistance and Peter Tyack, Doug Nelson, an anonymous referee and assorted colleagues for helpful comments on the manuscript. Funding was provided by National Science Foundation grants IBN-94-06217 and IBN-99-74527. References Baker, M. C. 2003. Local similarity and geographic differences in a contact call of the galah (Cacatua roseicapilla assimilis) in western Australia. Emu, 103, 233–237.

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