Experimental Evidence That Distinct Song Phrases in the Grey-Cheeked Fulvetta Alcippe Morrisonia Permit Species and Local Dialect Recognition

Ibis (2013), 155,32–41

Experimental evidence that distinct song phrases in the Grey-cheeked Fulvetta Alcippe morrisonia permit species and local dialect recognition

BAO-SEN SHIEH,1* SHIH-HSIUNG LIANG,2 HSIAO-WEI YUAN3 & CHAO-CHIEH CHEN1 1Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, 100 Shihchuan 1st Road, Kaohsiung, 807, Taiwan 2Department of Biotechnology, National Kaohsiung Normal University, 62 Sanchung Road, Yanchao Township, Kaohsiung, 824, Taiwan 3School of Forestry and Resource Conservation, National Taiwan University, No.1, Sec. 4, Roosevelt Road, Taipei, 106, Taiwan

Birds with small song repertoires have a limited number of song types which may serve multiple functions. The Grey-cheeked Fulvetta Alcippe morrisonia is a non-migratory species of lowland forests in Taiwan. Its song consists of two distinct phrases: a whistled phrase and a harmonic one. Each individual usually sings only one type of whistled phrase, and the geographical patterns of songs can be distinguished by the motif of this phrase. We proposed a dual adaptation hypothesis for the functions of these two phrases. Playback experiments including six sound stimuli (familiar whistled phrases, familiar harmonic phrases familiar complete songs, foreign whistled phrases, foreign harmonic phrases and foreign complete songs) were conducted at 12 sites in the Shoushan Nature Park of Kaohsiung, Taiwan. Grey-cheeked Fulvettas came closer to the playback speaker and increased counter-singing more in response to the familiar whistled phrase (local dialect) than to a foreign whistled phrase (distant dialect). However, birds responded equally to the playback of harmonic stimuli from familiar and foreign sources. We suggest that in this species, whistled phrases are used for local recognition and harmonic phrases are used for species recognition in short-range communication. Keywords: communication, experiment, repertoire, Taiwan.

Adaptation to function and environmental context 1988). Songs are also used for territory defence have been identified as the primary drivers of the and mate attraction, and both of these functions evolution of bird song acoustics (Kroodsma & may require the recognition of individuals and Miller 1982, Boncoraglio & Saino 2007). One local populations (Catchpole & Slater 1995). The important function of song is to enable birds to simultaneous need for both species specificity and recognize individuals of their own species (Catch- individual variability places potentially conflicting pole & Slater 1995). Features such as syntax, ele- demands on the evolution of bird songs (Marler ment structure and frequency, which vary little 1960). and are relatively constant among individuals of For species with medium to large song reper- the same species, have been shown to be the most toires (i.e. 6–200 song types) (Stoddard et al. important cues for species recognition in several 1991), different song types may be used to meet bird species (Becker 1982). For example, fre- the respective needs of species specificity and indi- quency changes are important in species recogni- vidual variability. Geographically widely distrib- tion among Field Sparrows Spizella pusilla (Nelson uted song types are typically those that function in species recognition (Becker 1982). For birds with *Corresponding author. small repertoires (i.e. only one or two song types), Email: [email protected] songs with different functions involve different

patterning and organization instead of distinct song proposed that tonal, frequency-modulated signals types. For example, the Chestnut-sided Warbler are optimal for long-range communication, and Dendroica pensylvanica has two song patterns: that wide-spectrum sounds with sharp amplitude accented, which contains a distinctive ending, and modulation and limited frequency modulation are unaccented, which does not (Kroodsma et al. optimal for short-range communication. 1989). The unaccented song is used primarily in The Grey-cheeked Fulvetta Alcippe morrisonia territorial defence, and the accented song is used morrisonia is a non-migratory subspecies endemic for mate attraction. to Taiwan (Collar & Robson 2007). It is found Local dialect recognition is known to play a key commonly in lowland forests (Chou et al. 1998) role in prezygotic reproductive isolation (Baker and forages in mixed-species ﬂocks (Chen & Hsieh 1982, Danner et al. 2011). Variability in songs is 2002). The Grey-cheeked Fulvetta is monogamous required for local dialect recognition. For songbirds and sexually monomorphic, and both sexes partici- with a small repertoire, a local dialect can be rec- pate in parental care (Lin 1996, Kuo 2000). A ognized in various parts of a song (e.g. in the typical song comprises two distinct phrases: the terminal trill of the song in the Puget Sound whistled phrase and the harmonic phrase. The White-crowned Sparrow Zonotrichia leucophrys spectrogram structure of the whistled phrase is pugetensis) (Nelson & Poesel 2007) or in acoustic tonal and whistle-like, whereas the harmonic cues with different degrees of individual variation phrase has a broad frequency range with many in the song (Skierczyński & Osiejuk 2010). harmonics (Fig. 1). All the songs of this species In addition to its function, environmental fea- contain the whistled phrase, but not all of them tures such as habitat structure affect signal trans- include the harmonic phrase. Grey-cheeked Fulv- mission and thus have profound effects on the ettas usually perform a single song type based on evolution of acoustic structures in bird songs the whistled phrase (Shieh 2004), and this species (Morton 1975). Birds use songs not only for long- is therefore considered a small-repertoire species. range communication but also for short-range We propose a dual adaptation hypothesis to communication; thus, short-range songs are explain the evolution of two distinct phrases in expected to differ acoustically from long-range the songs of the Grey-cheeked Fulvetta as a result songs (Titus 1998). Wiley and Richards (1982) of adaptation to function and environment. From

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Figure 1. Sources of sound stimuli used for the playback experiments: FT1–12 were collected from 12 different sites in the study park; OT was collected from an area with a foreign dialect in Shanping. The whistled phrase is labelled with ‘W’ and the harmonic phrase with ‘H’ on the spectrogram. FT4, FT5 and FT6 have identical syllable combinations in the whistled phrase.

the functional adaptation perspective, we predict and harmonic phrases from 12 different sites (all at that the whistled phrase is used for local recogni- least 50 m apart) in the study park and used one of tion, due to its consistency within individuals and the most common song types from Shanping its geographical variability (Shieh 2004), and the (recorded in 2004) as the source of our ‘foreign’ harmonic phrase is used for species recognition, sound stimuli. Because the Grey-cheeked Fulvetta due to its consistency across populations in differ- defends no obvious territorial boundaries and ent locations (B.-S. Shieh, pers. obs.). We there- because the nests of different pairs can be as close as fore predict stronger individual response to 5 m (Lin 1996), to ensure that the recordings from playback of the local whistled phrase than to the the 12 sites were from 12 different birds only one playback of whistled phrases from different dia- visible singing individual was recorded at each site, lects, but similar responses to harmonic phrases and it was followed until it flew out of recording irrespective of local or foreign sources. In addition, range. From each site, we selected only one high- according to Wiley and Richards’s (1982) proposi- quality recording of a source song with three sylla- tion for environmental adaptation, we predict that bles in the harmonic phrase. Recordings of the whistled phrases are used for long-range communi- source songs were digitized and filtered at 1 kHz cation because their tonal structure transmits effi- using Avisoft-SASLab Pro software (R. Specht, Ber- ciently across long distances, and harmonic phrases lin, Germany). The spectrographic cross-correlation are used for short-range communication due to (SPCC) coefficients were computed to investigate their wide spectrum structure. That is, from the the similarities between source songs using Avisoft- environmental adaptation perspective, the two CORRELATOR (sampling rate = 22050 Hz, distinctive phrases of this species’ song are used FFT = 512, frequency tolerance deviation = 0) for long-range and short-range communication, (Specht 2010). SPCC coefficients were calculated respectively. Therefore, we also predict that the as the two spectrograms shifted incrementally past Grey-cheeked Fulvetta will respond to short-range each other along the time axis and ranged from À1 signals (i.e. harmonic phrases) with short-range to +1. A value of +1 means that the two spectro- signals, and respond to long-range signals (i.e. grams were identical. Higher values of SPCC coeffi- whistled phrases) with long-range signals. Further- cients indicate a greater similarity between the two more, the Grey-cheeked Fulvetta should come sound spectrograms. This method was used because closer to the speaker during the playback of the comparisons are difficult to make using parametric harmonic phrase and counter-sing from a longer dis- methods (Cortopassi & Bradbury 2000). tance during the playback of the whistled phrase. Recordings of the 13 source songs (12 from the study park and one from the Shanping area) were prepared as 20-s playback files and categorized as METHODS having one of three types of sound stimuli: whistled phrases (W), harmonic phrases (H) or com- Study area and playback recordings plete songs (T). The 20-s sound stimuli of the We studied a Grey-cheeked Fulvetta population in separate whistled and harmonic phrases consisted the Shoushan Nature Park (22°38′N, 120°16′E) of of 10 evenly spaced phrases, and the 20-s sounds Kaohsiung City in southern Taiwan. The Shoushan of the complete songs consisted of five whistles Nature Park covers an area of approximately and five harmonic phrases to maintain periods of 1000 ha and reaches an altitude of 356 m above silence comparable to the whistled and harmonic sea level. The vegetation of the study area is char- playbacks (Fig. 2). acterized as evergreen rainforest. All of the sounds used in the playback experi- Playback procedures ments were recorded in the study park and in Shanping (22°58′N, 120°41′E), which is located We used a Denon Portable IC Recorder (DN- approximately 80 km from the study park. The F20R) connected to a wireless speaker (MIPRO sounds were recorded between 07:00 and 10:00 h MA-101, frequency response 50–15 000 Hz ± in 2005 using a Denon Portable IC Recorder (DN- 3 dB) for the playback experiments. The speaker F20R) equipped with a Sennheiser ME67 uni- was placed on a tree approximately 1–2 m above directional microphone. For the experiment, we the ground. Playback trials were conducted selected songs with good qualities of both whistled between 06:00 and 09:00 h, a period correspond-

a) kHz We broadcast two sets of sound stimuli at 12 10 sites in the study park. The familiar set of sound

5 stimuli was played back at the site in which it was recorded, and the foreign set of sounds originating from the Shanping area was played at all 12 sites. 5 10 15 s b) kHz Each set of sound stimuli included three types of 10 sound stimuli. Thus, each site received six sound stimuli: (1) familiar whistled phrases (FW), (2) 5 familiar harmonic phrases (FH), (3) familiar, complete songs (FT), (4) foreign whistled phrases 5 10 15 s (OW), (5) foreign harmonic phrases (OH) and (6) c) kHz foreign complete songs (OT) (Fig. 2). We used 10 complete songs as a positive control for our playback experiments using only whistled or harmonic 5 phrases. In each trial, the order of the sound stimuli was 5 10 15 s initially randomized within each set (familiar or d) kHz 10 foreign) and then counterbalanced so that each order occurred once in a trial. For example, the 5 played order of the sound stimuli in a trial could be FW-FH-FT, FH-FT-FW and FT-FW-FH. During each triplet, the ﬁrst sound stimulus was broadcast 5 10 15 s three times with silent intervals of 40, 40 and e) kHz 10 160 s. After a period of at least 2 min of silence (i.e. with no songs heard nearby), the second 5 sound stimulus was broadcast. Thus, in a single trial, each sound stimulus was played three times ﬁ 5 10 15 s in the rst, second and third place of the three- part sequence and was thus played a total of nine f) kHz 10 times. Because one trial lasted at least 65 min and the singing activity in the study park decreased 5 sharply after 09:00 h, we performed only two trials per day. The two trials for each day were con-

5 10 15 s ducted at two separate sites to avoid habituation effects. Trials with familiar and foreign sets of Figure 2. Examples of sound stimuli used for the playback sound stimuli were conducted at each site in the experiments at site 1: (a) familiar whistled phrase (FW); (b) late breeding season (May–July) of 2005 and familiar harmonic phrase (FH); (c) familiar complete song with another two trials with the same familiar and for- both whistled and harmonic phrases (FT); (d) foreign whistled eign sets of sound stimuli in the early breeding sea- phrase (OW); (e) foreign harmonic phrase (OH); and (f) foreign – complete song with both whistled and harmonic phrases (OT). son (March April) of 2006. Thus, playback experiments were repeated at two different times of the breeding season to increase the number of response samples while examining the effect of the ing to the peak in the natural song activity of time of the breeding season on the results. birds. After setting up the equipment, we waited until there was no disturbance and at least one Measurement of singing and approach Grey-cheeked Fulvetta was nearby. Sounds were response played back at a sound-pressure level of approximately 65 dB at 5 m from the speaker. Playback We considered a site to be our sampling unit, levels were adjusted to approximate the natural and all singing or approach responses of Grey- levels of a singing bird, depending on the habitat cheeked Fulvettas near the playback speaker at and wind conditions. the site were recorded. Aggressive responses

were not considered as they occurred only rarely Statistical analyses and call responses were not considered because they often occurred irrespective of playback. We Statistical analyses of responses to playbacks were used the ‘site’ instead of the ‘individual’ as the based on a repeated measures approach using linear sampling unit for two reasons. First, we did not mixed models (LMM). The type of sound stimulus identify individuals that sang or approached the (whistled, harmonic or complete), familiarity of playback area. Secondly, we expected that indi- the sound stimulus (familiar or foreign), and the viduals at the same site might respond similarly time of the breeding season (early or late) were to the same sound stimuli. However, responding entered as fixed factors in the models, and intra-site adults at the same site may often be different variation was taken into account by including the individuals due to the high annual mortality rate variable ‘site’ as a random factor. Model selection of adult Grey-cheeked Fulvettas (85.7% for sec- was based on backward selection from a full model, ond-year adults; Hu 1999). All song responses including all two- and three-way interactions. The were recorded and categorized as whistled (W), differences between pairs of stimuli were analysed harmonic (H) or complete songs (T) based on using a least significant difference post hoc compari- spectrograms (Fig. 1). We also calculated the fol- son of the estimated marginal means. lowing two measures for singing and approach We examined the association between response responses to the sound stimuli in a trial: (1) sound types and the type of sound stimulus, and proximity score and (2) occurrence percentage, whether this association depends on the time of as follows. We marked the horizontal distance the breeding season and familiarity of the sound from the speaker at 5 and 10 m. Using these stimulus using a hierarchical log-linear analysis marks, we estimated the distance between the procedure (SPSS Inc. 2003). We performed model speaker and a bird that was either singing or selection based on a backward elimination proce- approaching. The singing proximity score was dure with the probability of removal set at 0.1. In given a value of ‘1’ when songs were heard other words, we started with a saturated model, within a 20–30-m radius of the speaker during and each interaction was tested for significance by the playback period and the silent interval that deleting it from the model; these interaction terms followed, ‘2’ when within a 10–20-m radius, ‘3’ were removed from the model if the significance when within a 5–10-m radius and ‘4’ when probability for the change in chi-square for each within a 5-m radius. Vegetation structure limited effect was greater than 0.1, until only significant visibility so that approach behaviour could only terms remained. All analyses were conducted with be certainly recorded within 10 m of the SPSS version 14.0. speaker. The approach proximity score was thus ‘1’ when a bird approached within 5–10 m of RESULTS the speaker and ‘2’ when it came within 5 m. We used only the closest response to calculate Song characteristics proximity scores because birds might respond more than once during the playback period and The 12 source songs from the 12 sites in the study the following silent interval. We then summed park could be classified into 10 song types based the nine singing (or approach) proximity scores on the whistled syllables; three of the 12 source from the nine playbacks of the same sound songs had identical syllable combinations in the stimulus in a single trial to calculate the final whistled phrase (Fig. 1). The SPCC coefficients of singing (or approach) proximity scores and used the whistled phrases in the 10 song types ranged these in further statistical analyses. The final from 0.099 to 0.434, whereas the SPCC coeffi- proximity scores were natural logarithm-trans- cients between the whistled phrases in the foreign formed. song and in the 10 song types in the study park The occurrence percentage of singing (or ranged from 0.066 to 0.377. Amongst harmonic approach) during playbacks was calculated as the phrases, the two most similar source songs had an number of playbacks with the singing (or SPCC coefficient of 0.991 (Fig. 1), but with this approach) events divided by the total number of exception the coefficients ranged from 0.098 to playbacks in a trial (9). The occurrence percentage 0.385 within the study park, whereas the SPCC was arcsine-transformed for further analyses. coefficients between the harmonic phrases of the

foreign song and the phrases of the songs from the sound stimulus (LMM, proximity score: study park ranged from 0.069 to 0.179. The SPCC F4,137 = 2.53, P = 0.044; occurrence percentage: coefficients between the whistled phrases of the F4,137 = 3.96, P = 0.005). Specifically, harmonic foreign and familiar songs were significantly greater phrases provoked significantly less singing, and than those between the harmonic phrases of the responses occurred further from the playback foreign and familiar songs (Wilcoxon signed rank speaker than in the whistled and complete songs, test, n = 12, Z = À2.83, P = 0.005). but only during playbacks of familiar sound stimuli (Table 1). In addition, familiar harmonic phrases provoked singing responses similar to the response Singing response to playback to the foreign harmonic phrases, but familiar whis- The final LMM revealed that time of breeding tled phrases significantly increased singing responses season and familiarity of sound stimulus had signifi- compared with the foreign whistled phrases (Fig. 3). cant effects on the singing proximity score (time: The final log-linear model indicated a two-way F1,137 = 20.19, P < 0.001; familiarity: F1,137 = interaction (familiarity*type of sound stimulus: 27.17, P < 0.001) and on occurrence percent- df = 2, likelihood-ratio chi-square change = 24.46, age (time: F1,137 = 25.11, P < 0.001; familiarity: P < 0.001) and a three-way interaction (time of F1,137 = 20.59, P < 0.001). Playbacks conducted the breeding season*familiarity*response sound earlier in the season and of familiar song provoked type: df = 2, likelihood-ratio chi-square change = more and closer singing responses than playbacks 5.54, P = 0.063) (Goodness-of-fit test statistics for later in the breeding season and those of foreign the final log-linear model: likelihood-ratio chi song (Table 1). In addition, the two measures of square = 12.65, df = 20, P = 0.892; Pearson chi- singing responses were significantly influenced by square = 11.71, df = 20, P = 0.926). The three- the interaction between familiarity and type of way interaction demonstrated that the relationship between response sound type and familiarity was Table 1. Differences of least-square means in the final linear not the same at different times of the breeding mixed model for singing response. season (Fig. 4). Furthermore, response sound types did not have a significant interaction with the a ± SE Difference Estimate t137 P type of sound stimulus in the final log-linear model, indicating that the Grey-cheeked Fulvetta Proximity score Early vs. Late 0.70 ± 0.16 4.49 <0.001** responded with similar sound types regardless of Familiar vs. Foreign 1.08 ± 0.27 3.97 <0.001** the type of sound stimulus. Harmonic vs. Total À0.69 ± 0.27 À2.56 0.012* (Familiar) Whistled vs. Total À0.04 ± 0.27 À0.14 0.887 Approach response to playback (Familiar) fi Harmonic vs. Total 0.21 ± 0.27 0.77 0.444 Approach scores differed signi cantly between (Foreign) early and late in the breeding seasons (LMM, À ± À Whistled vs. Total 0.16 0.27 0.59 0.559 F1,137 = 5.67, P = 0.019) and between familiar (Foreign) and foreign sound stimuli (LMM, F1,137 = 20.33, Occurrence percentage < ± < P 0.001). Type of sound stimulus interacted sig- Early vs. Late 10.8 2.1 5.01 0.001** fi = Familiar vs. Foreign 12.1 ± 3.7 3.27 0.001** ni cantly with familiarity (LMM, F4,137 2.94, Harmonic vs. Total À10.5 ± 3.7 À2.83 0.005** P = 0.023). Specifically, in playback of foreign (Familiar) sound stimuli, harmonic phrases provoked signifi- Whistled vs. Total 3.0 ± 3.7 0.81 0.420 cantly closer approaches than whistled and com- (Familiar) plete songs, whereas playback of all three types of Harmonic vs. Total 1.9 ± 3.7 0.52 0.602 (Foreign) familiar sound stimuli provoked similar approach Whistled vs. Total À2.2 ± 3.7 À0.60 0.548 responses (Table 2, Fig. 3). In addition, familiar (Foreign) and foreign harmonic phrases provoked similar approach responses, whereas familiar whistled Early: early in the breeding season; Late: late in the breeding phrases provoked significantly closer approaches season; Familiar: sound stimulus from the same site; Foreign: sound stimulus from a distant population; Harmonic: harmonic than did foreign whistled phrases (Fig. 3). phrase; Whistled: whistled phrase; Total: complete song. The final linear mixed model for approach aEstimates of transformed data. **P < 0.01; *P < 0.05. occurrence only included the main effects of the

Table 2. Differences of least-square means in the ﬁnal linear (a) 2.5 mixed model for approach response. Familiar * * Foreign a ± SE Difference Estimate t137 P 2

Proximity score Early vs. Late 0.28 ± 0.12 2.38 0.019* 1.5 Familiar vs. Foreign 0.53 ± 0.20 2.60 0.010* Harmonic vs. Total 0.10 ± 0.20 0.48 0.629 (Familiar) 1 Whistled vs. Total 0.13 ± 0.20 0.63 0.531 (Familiar) Harmonic vs. Total 0.45 ± 0.20 2.20 0.029*

Ln (Sining proximity score) 0.5 (Foreign) Whistled vs. Total À0.23 ± 0.20 À1.10 0.272 (Foreign) 0 Occurrence percentage t141 Harmonic phrase Whistled phrase Complete song Early vs. Late 3.0 ± 1.3 2.33 0.021* Playback type Familiar vs. Foreign 5.3 ± 1.3 4.08 < 0.001** (b) 30 Early: early in the breeding season; Late: late in the breeding * season; Familiar: sound stimulus from the same site; Foreign: Familiar * Foreign sound stimulus from a distant population; Harmonic: harmonic 25 phrase; Whistled: whistled phrase; Total: complete song. aEstimates of transformed data. **P < 0.01; *P < 0.05. 20

15 time of the breeding season (F1,141 = 5.43, P = 0.021) and familiarity (F1,141 = 16.64, P < 0.001) and did not include interaction effects. Playbacks 10 early in the breeding season provoked more approaches than those late in the breeding season, 5 and playbacks of familiar sound stimuli provoked Arcsine (Singing occurrence percentage) more approaches than playbacks of foreign sound 0 Harmonic phrase Whistled phrase Complete song stimuli (Table 2). Playback type

(c) 1.4 DISCUSSION Familiar * * Foreign Whistled phrases for local recognition 1.2 in both long- and short-range 1 communication The whistled phrase is the initial phrase in Grey- 0.8 cheeked Fulvetta song and consists of three to five syllables with distinguishable motifs that show sig- 0.6 nificant geographical variation (Shieh 2004). The foreign stimuli used in the study originated 0.4 approximately 80 km from the study population and possess a combination of whistled syllables Ln (Approaching proximity score) 0.2 that are quite different from that of the study pop- 0 ulation (the SPCC coefficients ranged from 0.066 Harmonic phrase Whistled phrase Complete song to 0.377). The differential response to the familiar Playback type and foreign whistled phrases, consistent through the breeding season, demonstrated that Grey-chee- Figure 3. Estimated marginal means ± se of transformed data ked Fulvettas were able to use the whistled phrase for singing and approach responses in regarding with type of * < to discriminate between the local dialect and the sound stimulus and familarity during playback trials. P 0.05.

dialect identity, respectively (Nelson & Poesel 2007), we suggest that the whistled phrase–the introductory part of the Grey-cheeked Fulvetta’s song–may identify both local dialect and individual. The whistled phrase in the song of the Grey- cheeked Fulvetta is an effective cue for individual identity because it varies among individuals and is highly consistent with the stereotypy of each individual (Shieh 2004). To verify our suggestion,

Frequency further playback designs should test for individual recognition, and an analysis of the stability of individual cues across seasons (Wegrzyn et al. 2009) should be conducted. If the Grey-cheeked Fulvetta uses whistled phrases for long-range communication and harmonic phrases for short-range communication, we predicted that the birds would respond to Time of breeding season and sources of stimuli short-range signals (i.e. harmonic phrases) with short-range signals, and to long-range signals (i.e. Figure 4. Frequency of the three types of response sounds whistled phrases) with long-range signals. However, after playbacks of familiar or foreign sound stimuli during differ- we found no significant relationship between the ent times (early or late) of the breeding season. T, complete type of sound stimulus and the response sound song with both whistled and harmonic phrases; W, whistled types in playback experiments. Grey-cheeked Fulv- phrase; H, harmonic phrase. ettas were more likely to sing songs with whistled phrases regardless of the type of sound stimuli. distant dialect. Furthermore, we suggest that the Furthermore, when the stimuli were from familiar discrimination between local whistled phrases and sources, Grey-cheeked Fulvettas responded with foreign whistled phrases results from familiarity whistled phrases at close proximity. These results rather than non-similarity of acoustic structures. demonstrated that whistled phrases were used both Given that the SPCC coefficients between two as long- and short-range signals. whistled phrases in the study park ranged from 0.099 to 0.434, it is not unusual for neighbouring Harmonic phrases for species birds to sing very different whistled phrases. That recognition in short-range is, Grey-cheeked Fulvettas recognize dissimilar communication whistled phrases and counter-sing in response to those that are familiar (i.e. those of territorial The results indicated that Grey-cheeked Fulvettas neighbours). A lower singing response to foreign did not discriminate between foreign and familiar whistled phrases is associated with their unfamil- harmonic phrases. This lack of discrimination was iarity rather than the dissimilarity of their acoustic not due to acoustic similarities, given that the structures. Grey-cheeked Fulvettas can thus recog- SPCC coefficients between the harmonic phrases nize ‘familiar’ local whistled phrases even though of foreign and familiar song stimuli were often there are high levels of variations in those local smaller than those for the whistled phrase (0.069– whistled phrases. 0.179). However, it is possible that because the The Grey-cheeked Fulvetta’s use of the initial, SPCC analyses were conducted by cross-correlat- whistled phrase for local recognition differs from ing the time–frequency spectrograms of two that of other small-repertoire species, such as sounds and included all discernible structural fea- the Puget Sound White-crowned Sparrow, in tures of both sound spectrograms, the correlation which the terminal trill is used for dialect identity values of two harmonically rich sounds were more (Baptista 1977). Furthermore, whereas the Puget sensitive to overtone content and duration than Sound White-crowned Sparrow uses the note the tonal sounds (Khanna et al. 1997). Certainly, complex in the introductory phrase and the trill in the familiar and foreign harmonic phrases are simi- the terminal phrase as cues for individual and local lar when viewed as spectrograms (or as heard by

the human ear), and these tonal differences might Grey-cheeked Fulvettas approached the speaker explain why two harmonic phrases that seem because they recognized the foreign harmonic similar have smaller SPCC coefficients than phrases rather than because they were simply two whistled phrases that sound different. Grey- attracted by sounds; therefore, foreign harmonic cheeked Fulvetta individuals came close to the phrases but not foreign whistled phrases provoked playback speaker in response to both the foreign closer approaches. Moreover, our results revealed and the familiar harmonic stimuli, whereas they that the Grey-cheeked Fulvetta came close to the did not do so in response to the foreign whistled speaker during playback of harmonic stimuli from phrase. This provides evidence that the Grey-chee- both familiar and foreign sources. This finding ked Fulvetta recognizes foreign harmonic phrases. demonstrated that the Grey-cheeked Fulvetta used If harmonic phrases are used for species recog- harmonic phrases for short-range signals. nition, we would expect that the structures of the In conclusion, our results suggest that the whis- harmonic phrases would be relatively consistent tled and harmonic phrases in the song of the across different dialect areas in Taiwan as well as Grey-cheeked Fulvetta are used for local and spe- among different subspecies in other countries. cies recognition, respectively; the harmonic phrase Although we did not record songs from other sub- in the final part of the song is primarily used in species of the Grey-cheeked Fulvetta, one song short-range communication and is not mutually sample (recorded by David Farrow and accessible exclusive with the function of species recognition. at www.xeno-canto.org/19703) from a subspecies in Thailand showed similar harmonic syllables in We thank the administration of the Shanping Forest the final part of the song based on spectrograms. Ecological Garden of the Taiwan Forestry Research Insti- Additionally, Collar and Robson (2007) reported tute for its support during the study. We are very grate- ful to J. Wilson, L. Pichegru and anonymous reviewers that songs of the Grey-cheeked Fulvetta in all dis- for their valuable comments on earlier drafts of the tribution areas normally end with two to three manuscript. This work was supported by the Taiwan buzzy ‘eerh’ sounds, which are identified as har- National Science Council (grant no. NSC 93-2621-B- monic phrases in our study. The consistency of 037-001). harmonic phrases across populations may serve for both recognition of own species and distinction REFERENCES from congeneric, sympatric species. For example, the harmonic syllables make the songs of the Baker, M.C. 1982. Vocal dialect recognition and population – Grey-cheeked Fulvetta easily distinguishable from genetic consequences. Am. Zool. 22: 561 569. ’ Baptista, L.F. 1977. 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