The Song Structure of the Siberian Blue Robin Luscinia [Larvivora] Cyane and a Comparison with Related Species

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Ornithol Sci 16: 71 – 77 (2017)

ORIGINAL ARTICLE The song structure of the Siberian Blue Robin Luscinia [Larvivora] cyane and a comparison with related species

Vladimir IVANITSKII1,#, Alexandra IVLIEVA2, Sergey GASHKOV3 and Irina MAROVA1

1 Lomonosov Moscow State University, Biology, 119899 Moscow Leninskie Gory, Moscow, Moscow 119899, Russian Federation 2 M.F. Vladimirskii Moscow Regional Research Clinical Institute, Moscow, Moscow, Russian Federation 3 Tomsk State University-Zoology Museum, Tomsk, Tomsk, Russian Federation

ORNITHOLOGICAL Abstract We studied the song syntax of the Siberian Blue Robin Luscinia cyane, a small insectivorous passerine of the taiga forests of Siberia and the Far East. Males SCIENCE have repertoires of 7 to 14 (mean 10.9±2.3) song types. A single song typically con- © The Ornithological Society sists of a short trill comprised of from three to six identical syllables, each of two to of Japan 2017 three notes; sometimes the trill is preceded by a short single note. The most complex songs contain as many as five or six different trills and single notes. The songof the Siberian Blue Robin most closely resembles that of the Indian Blue Robin L. brunnea. The individual repertoires of Siberian Blue Robin, Common Nightingale L. megarhynchos and Thrush Nightingale L. luscinia contain groups of mutually associated song types that are sung usually one after another. The Siberian Blue Robin and the Common Nightingale perform them in a varying sequence, while Thrush Nightin- gale predominantly uses a fixed sequence of song types. The distinctions between the song syntax of Larvivora spp. and Luscinia spp. are discussed. The individual songs of Luscinia spp. are much more complex and are performed with less prolonged pauses than those of Larvivora spp.

Key words Avian song, Larvivora cyane, Syntax

The study of avian vocalisations significantly con- Weiss et al. 2014), Thrush Nightingale L. luscinia tributes to our understanding of evolutionary biol- (Sorjonen 1987; Naguib & Kolb 1992, Grieβmann ogy and taxonomy. Although advances in taxonomic & Naguib 2002; Ivanitskii et al. 2013; Marova et research are associated mostly with molecular genet- al. 2015) and Bluethroat L. svecica (Naguib & Kolb ics, comparative bioacoustic studies can also shed 1992; Turčoková et al. 2010). More recently, Alström light on the evolutionary relationships among spe- et al. (2013), and Song et al. (2014) have addressed cies and clarify the taxonomic structure of a selected briefly the songs of Blackthroat Luscinia obscura and group (Payne 1986; Alström & Ranft 2003). Firethroat L. pectardens. The songs of species in the genus Luscinia have The song of the Siberian Blue Robin (a small taiga attracted considerable attention due to their great forest passerine that ranges from West Siberia east- variety and their complex structure. As many as 18 ward to the Japanese islands), has never before been species are included in the genus Luscinia sensu lato, the subject of special research. Previously, only a but the taxonomic position and composition of this brief description of its song and data on its breeding genus still remain subjects of debate (Sangster et ecology and territorial behavior have been published al. 2010). Only a few species have been studied in (Tamura & Ueda 2001a, b). The aim of our research detail, from the perspective of bioacoustics; among was to describe the Siberian Blue Robin’s song in them are: Common Nightingale L. megarhynchos great detail and to conduct a comparison among dif- (Hultsch & Todt 1989; Sprau & Mundry 2010; ferent species of robins and nightingales, including the Indian Blue Robin L. brunnea, which has recently (Received 22 April 2016; Accepted 27 October 2016) been recognized as the closest relative of the Siberian # Corresponding author, E-mail: [email protected] Blue Robin (Sangster et al. 2010).

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index. The linearity index (index A) is the ratio of the MATERIALS AND METHODS number of song types in the repertoire to the number Our recordings were made with a Marantz PMD- of switches between different types of song. If the 660 recorder and a Sennheiser-IU 66 microphone vocal session is represented as a transition matrix, the near Krasnoyarsk (four males in “Stolby” State linearity index is calculated by dividing the number Reserve in 2009), in the Amur region (three males of rows by the number of cells filled with non-zero in “Khingansky” Reserve in 2013), in the Tomsk content (Scharff & Nottebohm 1991). The second Region (three males in 2014) and near Nachodka index (index B), a modified version of index A, is (seven males in 2004–2005). No playback was used, the ratio of the total number of the most frequent and each male was recorded only once. Forty-six transitions calculated for each song type to the total to 89 songs were recorded per male. The breeding number of transitions between all types of songs in status of most males was not controlled because of the vocal session. The limits and variation of both of their extreme caution and timidity. We used also the these indices are the same: from 1 (completely deter- recording of three males made in Kedrovaya Pad minate sequence; in each matrix row all transitions Reserve by BN. Veprintsev (in Veprintsev’s Phono- are concentrated in one cell) to a very small value theca of Animal Voices; catalogue numbers: 208605, (random sequence; transitions are distributed across 209632, 209642). For the comparative analysis we many cells in the row). used our own recordings of L. sibilans (eight males) made in the same areas and years (L. sibilans and L. RESULTS cyane often occur in the same habitat). The songs of L. luscinia (12 males) were recorded in Moscow The Siberian Blue Robin’s song is a short, loud (2010), and those of L. megarhynchos (23 males) in trill clearly separated by pauses. Each subsequent Ukraine (2013). Recordings of seven male L. brun- song normally belongs to a type different from the nea were obtained from www.xeno-canto.org (cata- previous one (immediate variety). Typical songs con- logue numbers and recordists: XC96490 D. Marques; tain three to five identical syllables, each consisting XC103690 D. Wagner; XC110069, XC111185 and of two or three notes (Fig. 1; 2, 10, 11, 12). In some XC110837 F. Lambert; XC20191 N. Athanas; songs, trills are preceded by single tonal introductory XC81053 Y. D. Li). notes (Fig. 1; 3, 4, 13). More complex songs may Song visualization and measurement was done contain up to five or six different vocal components using Syrinx 2.5s (JM. Burt: http://syrinxpc.com) (trills and single notes) (Fig. 1; 1, 5, 6). The reper- with 512 FFT and Blackman window. For each song toire of individual males includes 7–14 song types we measured: 1) maximum frequency (kHz); 2) mini- (average 10.9±2.3). A total of 134 song types was mum frequency (kHz); 3) frequency range (kHz); 4) identified, 57 in Siberia and 88 in the Far East, with song length (seconds); 5) pause length (length of the only 11 present in both groups. pause following the song; seconds); 6) total number The frequency band of singing is wide (1.7 to 8.8 of syllables; 7) number of syllable types. The mean kHz), but individual songs typically occupy a more values are presented below with standard deviations. limited range (Fig 1). One male may present different Data were processed in PAST v.2.15b (Hammer et song types in a completely different (non-overlap- al. 2001). To verify the differences between groups ping) range. The very slow pace of the singing is a we ran: two-tailed non-parametric MANOVA tests very distinctive feature. The pauses between songs with 9,999 permutations, Bray-Curtis measures are about ten times longer than the songs themselves for intra-group and between group distances, and (Table 1) and are usually filled with short (~ 30–40 Bonferroni corrections for multiple comparisons ms) sounds that lie in the narrow range (~ 250–300 (Anderson 2001). Hz) at a frequency of 4.9±0.18 kHz (Fig. 1; 8–11). For the syntax analysis we used four vocal ses- The duration of pauses between these sounds is about sions each for Siberian Blue Robin and Thrush 300 ms. The periodicity of sound emission remains Nightingale. First, a catalogue of song types was highly uniform during the whole singing. These quiet created for each male; then the complete sequence of sounds are characteristic of the Siberian Blue Robin’s song types was determined. We used two variables song, as previously described by Tamura and Ueda (indices) to describe the sequence of the different (2001a). The differences between the basic param- song types: a linearity index, and a modified linearity eters of the songs of Siberian Blue Robin and Indian

72 Avian song syntax

Fig. 1. Example sonograms of song types. 1–17 Siberian Blue Robin; 18–22 Indian Blue Robin; 23–25 Rufous-tailed Robin; 26–33 Common Nightingale; 34–35 Thrush Nightingale.

Blue Robin are highly significant (P<0.001) (see “sequenced” (see Fig. 2), with filling and framing Table 1). designating repeated clusters of song types. Some The vocal sessions of four male Siberian Blue clusters were performed more frequently than Robin and four male Thrush Nightingale were expected by chance alone. Consider, for example,

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Table 1. Basic parameters of the songs of Siberian Blue Robin and Indian Blue Robin.

L. cyane L. brunnea Song Parameters Mean±SD Limits Mean±SD Limits Maximum frequency, kHz 6.2±1.4 3.8–8.8 7.4±0.2 6.7–7.6 Minimum frequency, kHz 3.0±0.8 1.6–5.2 2.9±0.6 2.0–4.6 Frequency range, kHz 3.1±0.9 1.6–5.4 4.5±0.6 2.9–5.3 Song length, s 1.0±0.1 0.7–1.4 1.1±0.1 0.9–1.3 Pauses between songs, s 11.2±3.0 7.8–15.9 18.4±10.9 5.0–33.1 Number of syllables 6.5±2.8 2.0–17.0 6.4±1.7 4.0–10.0 Number of syllable types 1.6±0.6 1.0–4.0 2.4±0.7 1.0–4.0

Fig. 2. Sequences of different song types of four male Siberian Blue Robins A,( B, E, F) and four male Thrush Nightingales (C, D, G, H). Numbers indicate different song types. The same numbers for different males represent different songs type. Shaded and framed song types indicate repeating clusters (sequences of song types). the combination of song types 92 and 93 in male fact, there were six combinations of song types 92 B. Initially we assumed that they were performed and 93 among 55 paired combinations presented in independently. Given the number of times each was this vocal session. Thus, the observed frequency of performed (nine times for song type 92 and eight sequential execution of song types 92 and 93 was times for song type 93) and the total number of songs 0.11. According to Fisher’s exact test, the difference in this vocal session (56), the expected probability between observed and expected frequencies is sig- of their execution one after another in any order, is nificant (P=0.02). More complex clusters were also P=9/56 * 8/56=0.02. This means that one should repeated. For example, the vocal session of male D expect the appearance of only two combinations of contained three combinations of song types 9, 36, 42 song types 92 and 93 among 100 randomly selected and 44. Each time these song types were performed paired executions from the repertoire of this male. In immediately one after another, albeit in a variable

74 Avian song syntax sequence. The expected probability of such events is of execution of the various sequences, is also fixed about 1 out of 10,000 cases, a value that is negligibly (Ivanitskii et al. 2013). small compared with the observed frequency of this The differences in the syntactic organization of the combination. songs of Siberian Blue Robin and Thrush Nightingale Similar syntax patterns are obvious in the song are clearly identifiable in the positions of males syntax of all of the Siberian Blue Robin and Thrush against the two axes corresponding to the linearity Nightingale males studied. Apparently, the produc- indices (Fig. 3). The 75% ellipses encompassing the tion of different song types is not a purely random points representing these two species (each point process. Some song types are mutually associated corresponds to one male) do not overlap. The inter- and are usually performed together as a sequence or specific differences between the index values is sta- cluster. In the Siberian Blue Robin, the order of their tistically significant despite the very limited sample performance varies. In one case, the sequence may size (P=0.028; non parametric MANOVA with per- be performed as A → B → C, in another as B → A mutations). → C, or, alternatively, as C → B → A. The avail- able data suggest that one combination may include DISCUSSION at least four different song types. Longer recordings are needed to achieve a more complete and detailed The size of the individual repertoire of the Siberian picture. Blue Robin is very similar to that of the Thrush Unlike the Siberian Blue Robin, the Thrush Nightingale (Sorjonen 1987; Ivanitskii et al. 2013), Nightingale uses linear syntax. It sings individual whereas the repertoire of the Common Nightingale is songs, belonging to a given cluster, in a fixed order much more extensive, with one male performing as of (Figs. 2 C & 2 F). In the Thrush Nightingale, such many as 146–280 song types (Hultsch & Todt 1989; song types are usually executed one after another in a Sprau & Mundry 2010). strict sequence according to a fixed program that may Despite the differences in the repertoire size the include up to six song types. In most cases, sequence song syntax of Siberian Blue Robin and Common execution begins with the first type of song, but it Nightingale shows similar traits while the Thrush may end after any song in the sequence. The order Nightingale stands apart from them. Groups of mutually associated song types, which are usually performed one after another (song clusters), are present in the songs of all three species. However, the songs of these species have certain syntactic differences, mainly due to their adherence to predominantly linear (unidirectional) or combinatory (multidirectional) syntax. Syntactic organization in the song of the Common Nightingale has been investigated in detail (Hultsch & Todt 1989; Weiss et al. 2014). All of the song types composing the extensive repertoire of a single male are stored in its memory in short clusters (song packages). One package contains from two to seven (average four) song types. Songs belonging to one package are performed together more often than with other songs, but the order of their presen- tation, and the number of songs performed varies from case to case. Thus, the composition of a vocal session by a Common Nightingale is based on predominantly combinatory syntax, i.e. individual songs Fig. 3. Position of vocal sessions of the Siberian Blue Robin (lower left) and Thrush Nightingale (upper right) in the space in a package are combined relatively freely. It seems of two indices of linearity. Each point corresponds to one that the songs of Siberian Blue Robin and Common male. A and B are linearity indexes (see Methods for a full Nightingale are by-and-large similar with regard to description). their syntactic organization. Unlike these two species

75 V. IVANITSKII et al. the Thrush Nightingale mainly uses linear syntax, i.e. 2.4±0.7 s). When singing at maximum speed, these individual songs performed in a fixed order (Figs. 2 pauses are reduced to just 0.12–0.15 s. Such short C & 2 F). pauses, are comparable to the pauses between syl- Recent molecular research has indicated that the lables within a song (on average 0.130±0.05 s); how- genus Luscinia sensu lato is polyphyletic, thus while ever, the structure of individual song types remains assigning Siberian Blue Robin to the genus Larvivora well preserved (Ivanitskii et al. 2013). along with with L. akahige, L. brunnea, L. komadori, L. ruficeps, and L. sibilans is strongly advocated ACKNOWLEDGMENTS (Seki 2006; Sangster et al. 2010), while Thrush Nightingale, Common Nightingale, Bluethroat, and We are grateful to Olga Veprintseva for providing probably also L. [Irania] gutturalis are to be included us with recordings from the Veprintsev’s Phonotheca in the genus Luscinia sensu stricto. of Animal Voices. This study was supported by the The song of the Siberian Blue Robin bears a very Russian Foundation for Basic Research (15-29-02771 strong similarity to that of the Indian Blue Robin and 16-04-01721) and Russian Science Foundation (Fig. 1). In both species, one song usually includes (14-50-00029). three to six identical syllables, consisting of two to three notes each. Sometimes the song is preceded by REFERENCES a short monosyllabic note. In particular, each individual song of both species is preceded by a sequence Alström P & Ranft R (2003) The use of sounds in of short, quiet notes given in a very uniform manner. avian systematics and the importance of bird sound Both of these species typically sing at a very slow archives. Bull Brit Ornithol Club 123A: 114–135. pace with prolonged pauses between song phrases. Alström P, Song G, Zhang Y, Gao X, Holt PI, Olsson There is a slight difference between them, but only U et al. (2013) Taxonomic status of Blackthroat Cal- in the frequency parameters. The Indian Blue Robin liope obscura and Firethroat C. pectardens. Forktail sings in a frequency range that is somewhat narrower 29: 52–57. and apparently more constant (2.4–7.2 kHz) than that Anderson MJ (2001) A new method for non-parametric of the Siberian Blue Robin (1.6–8.9 kHz). In general, multivariate analysis of variance. Aust Ecol 6: 32–46. their basic song structure is surprisingly similar given Grießmann B & Naguib M (2002) Song sharing in neighboring and non-neighboring Thrush Night- their considerable difference in external appearance ingales (Luscinia luscinia) and its implications for (plumage coloration). Complete geographical isola- communication. Ethology 108: 377–387. tion could be one reason for the reduced divergence Hammer O, Harper DAT, Ryan PD (2001) PAST: Pale- in their songs. In contrast, the songs of the Siberian ontological statistics software package for education Blue Robin and the Rufous-tailed Robin, the geo- and data analysis. Paleontol Electron 4(1): 9. graphical ranges of which overlap extensively, are Hultsch H & Todt D (1989) Memorization and repro- much more different and they can be heard singing duction of songs in nightingales (Luscinia mega- side by side in the same habitat. rhynchos): evidence for package formation. J Comp In terms of bioacoustics, the most important dis- Physiol A 165: 197–203. tinction between the genera Larvivora and Luscinia Ivanitskii VV, Marova IM & Antipov VS (2013) Prin- is that the individual songs of the latter have a much ciples of construction and modes of differentiation in more complex structure. The typical song of Luscinia the song of Thrush Nightingale (Luscinia luscinia, consists of three to six trills (phrases) whereas the typ- Turdidae) in Moscow population. Zool J 92: 206– ical Larvivora song frequently contains only one trill 220 (in Russian with English summary). (phrase) preceded by one or two introductory notes. Marova IM, Ivlyeva AL, Veprintzeva OD & Ivanitskii A further difference concerns the overall rhythm of VV (2015) A comparative analysis of song differ- singing; successive song phrases of Larvivora are entiation in Thrush Nightingale (Luscinia luscinia) separated by pauses, which are much longer than the and Common Nightingale (Luscinia megarhynchos) song phrases. In contrast, the pauses between song within their ranges. Zool J 94: 1–10 (in Russian with pauses in Luscinia are generally shorter than their English summary). songs. For example, Thrush Nightingale songs are Naguib M & Kolb H (1992) Vergleich des Strophen- 1.5–14.0 s (average 6.2±2.8 s) long, while the pauses aufbaus und der Strophenabfolge an Gesängen von between their songs range from 0.2 to 7.3 s (average Sprosser (Luscinia luscinia) und Blaukehlchen (Lus-

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