Voice Breaking and Its Relation to Body Mass and Testosterone Level in the Siberian Crane (Leucogeranus Leucogeranus)

Journal of Ornithology (2020) 161:859–871 https://doi.org/10.1007/s10336-020-01773-w

ORIGINAL ARTICLE

Voice breaking and its relation to body mass and testosterone level in the Siberian Crane (Leucogeranus leucogeranus)

Anna V. Klenova1 · Maria V. Goncharova2 · Tatiana A. Kashentseva3 · Sergey V. Naidenko4

Received: 9 August 2019 / Revised: 28 February 2020 / Accepted: 17 March 2020 / Published online: 2 April 2020 © Deutsche Ornithologen-Gesellschaft e.V. 2020

Abstract Vocal development of cranes (Gruidae) has attracted scientifc interest due to its special stage, voice breaking. During voice breaking, chicks of diferent crane species produce calls with two fundamental frequencies that correspond to those in adult low-frequency and juvenile high-frequency vocalizations. However, triggers that afect voice breaking in cranes are mainly unknown. Here we studied the voice breaking in the Siberian Crane (Leucogeranus leucogeranus) and test its relation to the body mass and testosterone level. We analyzed 5846 calls, 39 body mass measurements and 60 blood samples from 11 Siberian Crane chicks in 8 ages from 2.5 to 18 months of life together with 90 body mass measurements and 61 blood samples from 24 Siberian Crane adults. The individual duration of voice breaking and dates of its onset, culmination and completion depended neither on the body mass nor on the testosterone level at various ages. But we found correlation between the testosterone level and mean deltas of percentages of the high and low frequency components in Siberian Crane calls between the closest recording sessions. We also observed some coincidence in time between the mean dates of voice breaking onset and the termination of body mass gain (at 7.5 months of age), and between the mean dates of voice breaking completion and the start of a new breeding season. Similar relations have been shown previously for some other crane species. We also showed for the frst time that the mean dates of voice breaking culmination correlated with the signifcant increase of the testosterone level (at 10.5 months of age). So, we suggest that voice breaking in cranes may be triggered by the end of chicks’ body growth, is stimulated by the increase of testosterone level and ends soon after adult cranes stop taking care of their chicks.

Keywords Vocal development · Biphonation · Body weight growth · Sex hormone level in adolescents · Non-passerine birds · Parent–ofspring interaction

Communicated by T. S. Osiejuk.

Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10336-020-01773-w) contains supplementary material, which is available to authorized users.

* Anna V. Klenova [email protected]

1 Department of Vertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Vorobievy Gory, 1/12, Moscow, Russia 119234 2 National Research Center for Hematology, Novy Zykovsky proezd 4a, Moscow, Russia 125167 3 Oka Biosphere State Nature Reserve, Oka Crane Breeding Centre, Brykin Bor, Lakash district, Ryazan region, Russia 391072 4 A.N. Severtsov Institute of Ecology and Evolution RAS, Leninskiy pr. 33, Moscow, Russia 119071

Vol.:(0123456789)1 3 860 Journal of Ornithology (2020) 161:859–871

Zusammenfassung Stimmbruch und dessen Beziehung zur Körpermasse und zum Testosteronspiegel beim Schneekranich (Leucogeranus leucogeranus) Die Stimmentwicklung bei Kranichen (Gruidae) hat aufgrund einer besonderen Phase, dem sogenannten Stimmbruch, wissenschaftliches Interesse geweckt. Während des Stimmbruchs erzeugen Küken verschiedener Kranicharten Rufe mit zwei Grundfrequenzen, die denen der tiefen Frequenzen der adulten und den hohen Frequenzen der juvenilen Vokalisation entsprechen. Die Auslöser, die den Stimmbruch bei Kranichen beeinfussen, sind jedoch weitgehend unbekannt. Wir untersuchten hier den Stimmbruch beim Schneekranich (Leucogeranus leucogeranus) und analysierten dessen Beziehung zur Körpermasse und zum Testosteronspiegel. Wir analysierten 5.846 Rufe, 39 Körpermassenmessungen und 60 Blutproben von 11 Schneekranichküken aus acht Altersklassen zwischen zweieinhalb und achtzehn Lebensmonaten sowie 90 Körpermassenmessungen und 61 Blutproben von 24 adulten Schneekranichen. Die individuelle Dauer des Stimmbruches und die Zeitpunkte des Beginns, Höhepunkts und Abschlusses waren weder von der Körpermasse noch vom Testosteronspiegel in den verschiedenen Altersklassen abhängig. Wir fanden jedoch eine Korrelation zwischen dem Testosteronspiegel und den durchschnittlichen Deltas der prozentualen Anteile von hoch- und niederfrequenten Komponenten in Schneekranichrufen zwischen den direkt aufeinanderfolgenden Aufnahmen. Wir beobachteten auch eine gewisse zeitliche Überschneidung zwischen dem durchschnittlichen Zeitpunkt des Beginns des Stimmbruchs und der Beendigung der Körpermassenzunahme (im Alter von siebeneinhalb Monaten) sowie zwischen dem mittleren Zeitpunkt des Abschlusses des Stimmbruchs und dem Beginn einer neuen Brutsaison. Ähnliche Beziehungen konnten bereits für einige andere Kranicharten nachgewiesen werden. Weiterhin konnten wir zum ersten Mal zeigen, dass der mittlere Zeitpunkt des Höhepunkts des Stimmbruchs mit dem signifkant ansteigenden Testosteronspiegel korrelierte (im Alter von zehneinhalb Monaten). Wir vermuten daher, dass der Stimmbruch in Kranichen möglicherweise durch das Ende des Körperwachstums der Küken ausgelöst, durch den ansteigenden Testosteronspiegel angeregt wird und kurz nachdem die adulten Kraniche mit der Versorgung der Küken aufhören endet.

Introduction In other species, fundamental frequency in calls can remain relatively stable over chick development (up to Due to an active growth in the number of bioacoustical fedging or even later), after that it drops from high juvenile researches in the recent decades, more and more atten- values to low adult ones without correlation with the size of tion is being paid to the diversity of the patterns of vocal the chick’s body or syrinx (e.g., Gruiformes: Wilkinson and development, their underlying physiological mechanisms Huxley 1978; Niemeier 1979; Cosens 1981; Gebauer and and biological role in various groups of birds and mam- Kaiser 1998; Budde 2001; Hudiakova 2002; Klenova et al. mals. However, most studies on vocal development concern 2007, 2010, 2014; Charadriiformes, Alcidae: Klenova and vocal learning in birds and, particularly, the acquisition of Kolesnikova 2013; Procellariiformes: Naugler and Smith mature vocal patterns through listening to adult tutors (e.g. 1992; Duckworth et al. 2009; and some others: Riska 1986; Catchpole and Slater 2008; Marler and Slabbekoorn 2008). Baker et al. 2003; Radford 2004; Marques et al. 2010; Drag- At the same time, patterns of vocal development in species onetti et al. 2013). However, the morphological and physi- that do not learn their vocalizations could be quite diverse ological basis of this process is unclear. and complex as well, and need much more study. Among the species with jump-like vocal development, Variation in vocal development across the species that the transition from high-frequency juvenile to low-frequency lack vocal learning can be illustrated with the change of adult calls has been studied predominately in cranes (Grui- the call fundamental frequency. In some species, the fun- dae). Retention of high-frequency juvenile calls until the frst damental frequency declines gradually with age in relation autumn migration, and in some cases even in the winter, time to the body and syrinx growth (Würdinger 1970). Such a has been reported for six crane species out of 15: for San- pattern was reported for Anseriformes (Würdinger 1970; dhill (Grus canadensis), Eurasian (G. grus), Grey Crowned ten Thoren and Bergmann 1986, 1987; Engländer and (Balearica regulorum gibbericeps), Siberian (G. leucogera- Bergmann 1990), Galliformes (Garskaia and Chernyi 1979; nus), Red-crowned (G. japonensis) and Demoiselle Cranes Meinert and Bergmann 1983), Charadriiformes, Recurviro- (Anthropoides virgo; Niemeier 1979; Gebauer and Kaiser stridae (Adret 2012), Falconiformes (Smallwood and Duda- 1998; Budde 2001; Hudiakova 2002; Klenova et al. 2007, jek 2003; Marchenko et al. 2018) and some others (Redondo 2010, 2014). After completion of the active growth of the body 1991), though gradual syrinx development was shown only and vocal apparatus, the chicks of these species continue to for some Anseriformes species (Würdinger 1970). produce calls with a high fundamental frequency (Niemeier 1979; Klenova et al. 2007). At the same time, the fundamental

1 3 Journal of Ornithology (2020) 161:859–871 861 frequency characteristics of vocalizations of adult cranes are dates ranged from 15 to 31 May in 2012 (8 chicks) and from much lower than those of young cranes for each species (Nie- 17 to 25 May in 2013 (3 chicks). All chicks were human- meier 1979; Gebauer and Kaiser 1998; Budde 1999a, b; Bra- raised in the Oka Crane Breeding Centre of Oka State Nature gina and Beme 2007; Klenova et al. 2010, 2014). In cranes, the Biosphere Reserve (Ryazan region, Russia). Chicks were jump-like transition from juvenile high-frequency calls to adult housed in 25–100 m2 enclosures covered with grass, trees low-frequency ones has been referred to as “voice breaking” and bushes. Chicks were kept in individual enclosures for (Heinroth 1927; Niemeier 1979). At this age, young cranes the frst 1.5 months of their lives, after that they were joined emit calls containing simultaneously two independent funda- with conspecifcs in groups of 2–8 individuals. The subject mental frequencies: high juvenile and low adult ones. Then the chicks were sexed with DNA PCR-amplifcation (Grifths high-frequency component vanishes slowly, and after some et al. 1998) and individually marked with leg rings. All time a bird has only the low mature frequency component studied chicks were reared in the Breeding Centre for the (Niemeier 1979; Klenova et al. 2007, 2010, 2014). purpose of reintroduction, and all of them were successfully Previously, it has been shown that the onset of voice released into the wild at the age of 6–18 months. breaking varies both between diferent crane species (from We recorded calls in the morning, when the cranes were 2 months in the Demoiselle Crane to 7 months in the Red- most active. Each recording of a particular crane lasted crowned Crane), and individually within a single species, 20–40 min and was separated from another recording of depends neither on hatching date nor on clutch order nor the same bird by 24–48 h. During a recording session we on chick sex or weight. However, it roughly corresponds to made 1–4 recordings and recorded at least 16 calls per bird the period in which active body growth fnishes (Niemeier during a recording session. During the study, one bird was 1979; Bragina 2004; Klenova et al. 2010, 2014). Completion recorded only once, while the others—several times (3–8 of the voice breaking occurs in diferent species at nearly recording sessions per bird). On average, call recordings the same time (at 11–13 months) and corresponds in time to were made at the ages of 2.5, 5, 6.5, 7.5, 9.5, 10.5, 12.5 and the disruption of a parent-chick bond in the wild (Niemeier 18 months ± 10 days (Table 1). 1979; Klenova et al. 2010, 2014). Despite a lot of data col- We used a Marantz PMD-660 digital recorder (sampling lected on voice breaking in cranes, we still do not know the frequency 48 kHz) with a single AKG-C1000S (AKG- physiological mechanism for the voice breaking. Also, the Acoustics GmbH, Vienna, Austria) cardioid electret con- relation between the onset of voice breaking and the fnish denser microphone. The system had a frequency response of of active body growth has only been tested for two species 0.04–14 kHz. The distance from the bird to the microphone so far (Red-crowned and Demoiselle Cranes—Klenova et al. was 2–10 m. Calls were analyzed using Avisoft SAS-Lab 2010, 2014), and needs to be tested on a wider range of Pro v. 5.1.23 (Avisoft Bioacoustics, Berlin, Germany). To species. increase frequency resolution of sound display, the calls The subject species of our study is the Siberian Crane. were downsampled to 22.05 kHz. In order to be sure that It has Critically Endangered status in the IUCN Red List the observed frequency bands on the spectrograms were not (https://www.iucnredlist.org) and its population in the wild a result of aliasing, we used a 12 kHz low-pass flter prior is estimated at 4000 (Li et al. 2012), therefore any informa- to downsampling (antialiasing fltering). We created spec- tion about its biology is extremely important for conserva- trograms with a 1024-point Hamming window, frame 50%, tion and reintroduction eforts improvement. In this paper overlap 96.87%, providing time resolution of 1.45 ms and we analyzed vocal development of Siberian Crane which frequency resolution of 22 Hz. The recordings will be avail- has not been studied enough so far. We tested development able at https://www.animalsoundarchive.org. of calls, body mass growth and testosterone level changes in To estimate the approximate onset, culmination and com- parallel. Our objectives were to (1) describe voice breaking pletion of voice breaking, we used all the available record- in time line; (2) describe the process of body mass gain and ings from all the studied chicks, 16–100 noise-free calls per changes of testosterone level during the frst year of life; recording session per chick, 5846 calls in total (Table 1). For and (3) analyze their temporal relation to voice breaking in each call, we measured the total duration (Dur_total), the Siberian Crane. duration of the juvenile high fundamental frequency component (Dur_f0) and the duration of adult low fundamental frequency component (Dur_g0, Fig. 1). When the high or Methods the low fundamental frequency component included two or several fragments, the duration of this component were cal- Call recordings and analysis culated as a sum of the durations of each of these fragments. We also calculated percentage of each of the components The Siberian Crane calls were recorded in 2012–2014 from in the whole call as Perc_f0 = Dur_f0*100%/Dur_total or 11 individuals (8 males, 3 females). The chicks’ hatching Perc_g0 = Dur_g0*100%/Dur_total. Then we calculated

1 3 862 Journal of Ornithology (2020) 161:859–871

Table 1 The studied Siberian Crane chicks, their date of birth, number of measured calls and analyzed blood samples (in brackets) in each age Chick’s name and sex Date of birth Ages (months) 2.5 5 6.5 7.5 9.5 10.5 12.5 18

1. Argun ♂ 15.05.2012 41 (1) 100 (1) 100 (1) 100 (1) 100 (1) 100 (1) 68 (1) 58 (1) 2. Vorona ♂ 17.05.2012 52 (1) 100 (1) 100 (1) 100 (1) 100 (1) 32 (1) 16 3. Lena ♀ 18.05.2012 69 (1) 100 (1) 94 (1) 100 (1) 100 (1) 100 (1) 64 (1) 100 (1) 4. Uvat ♂ 19.05.2012 40 (1) 100 (1) 100 (1) 100 (1) 85 (1) 100 (1) 19 (1) 5. Savala ♂ 22.05.2012 100 (1) 100 (1) 100 (1) 100 (1) 100 (1) 100 (1) 6. Izhma ♂ 23.05.2012 100 (1) 7. Para ♂ 28.05.2012 100 (1) 98 (1) 100 (1) 100 (1) 8. Lel ♂ 31.05.2012 100 (1) 100 (1) 100 (1) 100 (1) 100 (1) 100 (1) 31 (1) 9. Taz ♂ 17.05.2013 100 (1) 100 (1) 100 (1) 100 (1) 100 97 82 (1) 10. Vasyugan ♀ 22.05.2013 100 (1) 100 (1) 100 (1) 11. Vakh ♀ 26.05.2013 100 (1) 100 (1) 100 (1) 100 (1) 100 100 100 (1) mean percentages of high and low components (Mean_ considered as onset of the voice breaking. The frst date Perc_f0 or Mean_Perc_g0) as mean values of Perc_f0 or when all recorded calls contained only adult low fundamen- Perc_g0 for all the measured calls of an individual chick tal frequency component (g0), was considered as completion within the recording session. We also calculated the mean of the voice breaking. The frst date when Mean_Perc_g0 deltas of each of the components between the closest record- was ≥ 20% was considered as culmination of voice breaking. ing sessions (e.g. ΔMean_Perc_ f0 = Mean_Perc_f0 in the We calculated duration of voice breaking as the diference given recording session—Mean_Perc_f0 in the previous between the completion and the onset of voice breaking, and recording session). the duration of the frst phase—as the diference between the Previously, two main call types (trills and chirps) for culmination and the onset of voice breaking. Siberian Crane chicks were reported (Hudiakova 2002). We measured acoustic variables of calls regardless of their type. Blood samples collection and enzyme immunoassay We used the defnition of voice breaking following Klenova et al. (2010, 2014) and identify this period as a time when We collected blood samples from the same 11 chicks in the a chick produces calls with both the juvenile high and the same ages when we recorded their calls (Table 1). We took adult low fundamental frequency components (f0 and g0, about 1–2 ml of blood from either right jugular or medial respectively). So, the frst date when at least one call with metatarsal vein (Olsen et al. 1996). We incubated the whole two frequency components (f0 and g0) was detected, was blood sample at + 4 °C for 20 min, after that we centrifuged

Fig. 1 The spectrogram illustrates the call pattern occurring before, the third call (c) two fundamental frequencies f0 and g0 are present during and after voice breaking in Siberian Crane: (a) only a high simultaneously that resulted in their interaction with appearance of fundamental frequency component f0 is present; (b), (c), (d) both a linear combinatory frequency bands. All calls are from male #9 of high f0 and a low g0 fundamental frequency components are present; 5.5–12.5 months old. The measured acoustic variables (Dur_f0 and (e) only a low fundamental frequency component g0 is present. In Dur_g0) are also shown

1 3 Journal of Ornithology (2020) 161:859–871 863 it at 1000×g (3000 rpm) for 20 min more. The obtained serum samples were collected in clear 2 ml Eppendorf tubes and kept frozen at − 18 °C until testosterone assessment. In total, we collected and analyzed 60 serum samples from the birds aged from 2.5 to 18 months (Table 1) and 61 samples from 24 adult cranes. Blood samples of adult birds were collected in three successive years (2012, 2013, 2014) at the end of October during the annual mass health examination of cranes. Since for the most of the adult Siberian Cranes we took blood samples multiple (two or three) times, later we used the mean individual value of testosterone level for each bird across all collected samples. Laboratory analysis was conducted at A.N. Severtsov Institute of Ecology and Evolution, Moscow, at the Collab- Fig. 2 Change in optical density of the standard curve and serially orative Usage Centre “Live collection of wild mammalian diluted serum sample from the Siberian crane with an initial concentration of 8.7 ng/ml (kit standards: y = − 1.95x + 0.878; samples: species.” We assessed testosterone concentrations directly y = − 1.89x + 1.263). Closed circles: testosterone kit standards, open in serum by ELISA commercial kits («Immunofa-TS», circles: diluted serum sample Immunotech, Russia) following the manufacturer guidelines and using Multiskan EX microplate reader (Thermo Fisher Scientifc, MA, USA). We measured the optical density at sessions and additionally, at the age of 4 months. Body mass wavelengths of 450 and 620 nm. According to the speci- of adult birds (14 males and 10 females from 2.5 to 37 years fcation, cross-reactivity of antibodies to testosterone was old) was registered each year at the end of October during 9% to 5-dehydrotestosterone, 1% to 11-hydrooxitestoster- the annual mass health examination of cranes. For analysis one and 5,5,-androstan-3,17-diol, and less than 0.01% to all we used mean values for several years (from 3 to 7 measure- other tested steroids. Sensitivity of the kits was 0.058 ng/ml. ments per bird). To weigh small chicks (to the nearest 10 g), To assess coefcient of variation (CV), we measured each we used MK-15.2-A20 weighing balance (Massa-K, Sankt- sample in duplicates of 20 µl. If CV was greater or equal Petersburg, Russia), and to weigh older chicks and adults (to to 5%, we redid the measurement, if CV was less than 5%, the nearest 50 g), we used M-ER 333BF “Farmer” balance we used a mean value of the two measurements for further (Mercury Wp Tech Group Co., Ltd., Seoul, Korea). analysis. Interplate CV was 3.72% (n = 2), intraplate CV was 1.79 ± 0.13% (n = 80). To determine whether this ELISA kit Statistical analyses can be used to measure serum testosterone in Siberian crane, we performed a parallelism test. We did not have serum sam- All the analyses were carried out with STATISTICA 8.0 ples of Siberian cranes with high testosterone concentration, software package (StatSoft, Inc., Tulsa, OK, USA). We used so we chose the sample with non-detectable testosterone one-way ANOVA with Tukey HSD post hoc tests to compare concentration (close to 0) and added testosterone to it for the body mass and testosterone level values across cranes the fnal concentration of 8.7 ng/ml. Then we serially diluted of diferent ages, as the distribution was normal at every the sample (1:1) with the same crane serum sample (0 ng/ age (Kolmogorov–Smirnov test, P > 0.05). For these values, ml). The standard curve followed the plasma dilution curve Mean ± SD are given everywhere. We used Mann–Whitney in a parallel manner (Fig. 2), indicating that the ELISA kits U-test to compare the mean percentages of high and low measured testosterone concentrations accurately. frequency components across cranes of diferent ages, as the distribution was not normal at every age (Kolmogo- Body mass measurement rov–Smirnov test, P < 0.05). For these values, Mean ± SE are given everywhere. We also computed the Spearman correla- Body mass measurements were made in 2003–2015 at Oka tion between the onset, culmination, completion, duration Crane Breeding Centre for the total sample of 94 birds. of the voice breaking and its frst phase and the chick body Chicks (29 males, 17 females and 31 chicks of unknown mass at the age of 2.5, 4, 7.5, 9.5 months and testosterone sex) were weighted on the day of hatching and then at the level at the age of 2.5, 5, 6.5, 7.5, 9.5, 10.5 months. We cal- age of 1, 2, 3, 4, 5, 7.5, 9.5 and 18 months. Body mass of culated the Spearman correlation between the mean percent- some chicks (n = 22) was measured once in one of the stated ages of high and low frequency components and their del- ages, while body mass of the other ones—repeatedly, in sev- tas (Mean_Perc_ f0, Mean_Perc_g0, ΔMean_Perc_ f0 and eral stated ages. We also measured the body mass of our 11 ΔMean_Perc_g0) and testosterone level values for the whole subject Siberian Crane chicks during almost all recording sample and for each chick separately as well. We used the

1 3 864 Journal of Ornithology (2020) 161:859–871 sequential Bonferroni method (Rice 1989) to determine statistical signifcance of our multiple correlation analyses, but we report all the correlations for which P values were below 0.05 to avoid being too conservative (Moran 2003). To compare the efects of factors “individual” and “testosterone” on the mean percentages of high and low frequency components and their deltas (Mean_Perc_ f0, Mean_Perc_g0, ΔMean_Perc_ f0 and ΔMean_Perc_g0), we used GLMM (with testosterone as the fxed factor and individual as the random factor).

Results

Changes of testosterone level through the development of Siberian Cranes

Although the chicks’ testosterone level increased signifcantly with age (one-way ANOVA, F8,92 = 3.2, p < 0.003), we did not fnd signifcant diferences in the level of testosterone in the most comparisons (Fig. 3a). At the age of 2.5–9.5 months, the level of testosterone of the Siberian Crane chicks was relatively stable (0.24 ± 0.17 ng/ml at 2.5 months, 0.22 ± 0.14 ng/ml at 9.5 months), but increased signifcantly to the age of 10.5 months (to 0.47 ± 0.23 ng/ml, post-hoc Tukey HSD test, p = 0.041), after that it decreased slightly to the age of 18 months (to 0.22 ± 0.12 ng/ml) and then gained higher values in adulthood. At the end of breeding season, testosterone level in adults was 0.46 ± 0.22 ng/ml Fig. 3 Changes of testosterone level (a), body mass (b) and mean (males 0.51 ± 0.28 ng/ml, N = 12, females 0.42 ± 0.12 ng/ml, percentages of high f0 (white boxes) and low g0 (grey boxes) funda- N = 12, Student’s T-test, F = 4.45, p = 0.02; Fig. 3a, Table 2). mental frequency components (c) with age together with approximate age of onset and culmination of voice breaking in Siberian Cranes. Changes of body mass through the development The middle points show the averages; box—SD for a and b and SE for c; whiskers—minimum and maximum values; the n near the of Siberian Cranes whiskers is a number of individuals included into the age period; *— shows signifcant diference (post hoc Tukey HSD test P < 0.05 for a At hatching, body mass of the Siberian Crane chicks was and b, Mann–Whitney U-test P < 0.05 for c) between ages. “onset”, culmination 0.13 ± 0.01 kg, then it increased rapidly to the age of “ ”—means ± sd age of onset and culmination of voice breaking in studied Siberian Crane chicks 7.5 months, after that it decreased slightly and plateaued out (Fig. 3b, Table 2). Although the chicks’ body mass increased signifcantly with age (one-way ANOVA, F9,226 = 480.8, (Niemeier 1979; Klenova et al. 2010, 2014): in autumn, p < 0.001), we did not fnd signifcant diferences in body chicks produced mainly calls with the juvenile high funda- mass in all the comparisons between ages greater than mental frequency component only (Fig. 1a; Online Resource 7.5 months (Fig. 3b). For example, body mass of 7.5-month- 1), in winter or early spring they started to produce calls old cranes (7.31 ± 0.38 kg) did not difer signifcantly from with both juvenile high and adult low fundamental fre- the mass of 9.5-month-old ones (7.09 ± 0.37 kg, post- quency components (Fig. 1b–d; Online Resource 2) and in hoc Tukey HSD test, p = 0.99) or from the mass of adults the end of spring or in summer they produced mainly calls (6.81 ± 0.65 kg, post-hoc Tukey HSD test, p = 0.30). with the adult low fundamental frequency component only (Fig. 1e; Online Resource 3). The ages of onset, culmina- Voice breaking and its relation to testosterone level tion and completion of the voice breaking varied greatly for and body mass in Siberian Cranes diferent Siberian Crane chicks, but on the average came to 7.7 ± 1.8, 9.2 ± 1.7 and 12 ± 2 months correspondingly We found that, in general, vocal development in Siberian (Table 3). Durations of the voice breaking and its frst phase Crane chicks goes similar to other studied crane species were 5.3 ± 1.8 and 1.7 ± 1.5 months correspondingly. Our

1 3 Journal of Ornithology (2020) 161:859–871 865

Table 2 Chick body mass and testosterone level (mean ± sd) at difer- mination, completion, total duration and duration of the frst phase of ent ages for all chicks and separately for males and females and the voice breaking Spearman correlation (r, p) between them and the age of onset, cul-

X mean ± sd (n) Correlation Correlation Correlation Correlation Correlation Age (months) for all chicks/ between X and between X and between X and between X and between X and males/females onset of voice culmination of completion of duration of voice duration of frst breaking voice breaking voice breaking breaking phase of voice breaking

Body mass (kg) 2.5 4.24 ± 0.39 (10)/ r = − 0.46 r = 0.17 r = − 0.29 r = 0.07 r = 0.14 4.37 ± 0.30 (7)/ p = 0.19 p = 0.65 p = 0.53 p = 0.88 p = 0.72 3.94 ± 0.46 (3) 4 6.31 ± 0.49 (10)/ r = − 0.55 r = 0.24 r = − 0.47 r = − 0.18 r = 0.69 6.46 ± 0.44 (7)/ p = 0.10 p = 0.53 p = 0.29 p = 0.70 p = 0.04 5.97 ± 0.52 (3) 7.5 7.31 ± 0.38 (10)/ r = 0.12 r = 0.49 r = 0.02 r = 0.18 r = − 0.19 7.40 ± 0.34 (7)/ p = 0.75 p = 0.19 p = 0.97 p = 0.70 p = 0.62 7.11 ± 0.45 (3) 9.5 7.09 ± 0.37 (7)/ r = − 0.02 r = − 0.07 r = − 0.95 r = − 0.80 r = − 0.14 7.11 ± 0.40 (6)/ p = 0.97 p = 0.88 p = 0.01 p = 0.10 p = 0.76 6.70 (1) Testosterone level 2.5 0.24 ± 0.17 (9)/ r = − 0.30 r = − 0.20 r = − 0.62 r = − 0.60 r = 0.12 (ng/ml) 0.23 ± 0.20 (7)/ p = 0.47 p = 0.63 p = 0.19 p = 0.21 p = 0.78 0.31 ± 0.09 (2) 5 0.29 ± 0.13 (9)/ r = − 0.42 r = 0.42 r = − 0.63 r = − 0.61 r = 0.17 0.28 ± 0.09 (6)/ p = 0.26 p = 0.30 p = 0.19 p = 0.22 p = 0.69 0.31 ± 0.21 (3) 6.5 0.33 ± 0.31 (10)/ r = − 0.04 r = − 0.08 r = − 0.62 r = − 0.57 r = 0.34 0.26 ± 0.14 (7)/ p = 0.91 p = 0.83 p = 0.14 p = 0.18 p = 0.37 0.49 ± 0.45 (3) 7.5 0.30 ± 0.26 (9)/ r = 0.30 r = 0.29 r = − 0.09 r = − 0.20 r = 0.14 0.20 ± 0.16 (7)/ p = 0.43 p = 0.49 p = 0.87 p = 0.70 p = 0.73 0.66 ± 0.15 (2) 9.5 0.22 ± 0.14 (8)/ r = 0.48 r = 0.55 r = − 0.79 r = − 0.77 r = 0.00 0.23 ± 0.15 (6)/ p = 0.23 p = 0.16 p = 0.06 p = 0.07 p = 0.99 0.18 ± 0.16 (2) 10.5 0.47 ± 0.23 (7)/ r = 0.01 r = − 0.52 r = 0.53 r = 0.30 r = − 0.29 0.46 ± 0.24 (6)/ p = 0.98 p = 0.23 p = 0.36 p = 0.62 p = 0.53 0.56 (1)

Statistically signifcant relations detected by Spearman correlation are indicated in bold; however these relations became insignifcant after sequential Bonferroni correction sample did not allow us to compare the parameters of voice 14.0 ± 9.6% at 12.5 months for Mean_Perc_high and breaking in males and females statistically due to the small 52.4 ± 12.5% at 10.5 months, 92.7 ± 7.0% at 12.5 months number of females among the studied cranes; however, in for Mean_Perc_low). From 12.5 to 18 months, the mean per- general, we did not notice any signs of sexual diferences in centage of high frequency component slowly came to zero, our study species (Table 3). while the mean percentage of low frequency—to 100%, Although the chicks’ mean percentages of high and low which meant the completion of voice breaking in Siberian frequency components changed considerably with age, we Cranes (Fig. 3c). did not fnd signifcant diferences in most comparisons We did not fnd signifcant correlation between onset, cul- (Mann–Whitney U-test, p > 0.05; Fig. 3c). From 2.5 to mination, completion, duration of the voice breaking and 10.5 months, the mean percentage of the high frequency its frst phase and a chick’s body mass at the age of 2.5, component decreased slowly, while the mean percentage of 4, 7.5 and 9.5 months and testosterone level at the age of the low frequency component increased slowly (Fig. 3c). 2.5, 5, 6.5, 7.5, 9.5 and 10.5 months (Table 2). We found Statistically significant changes occurred only between only a weak negative correlation between body mass at 10.5 and 12.5 months both for mean percentages of high and 9.5 months and completion of voice breaking, and a weak low frequency components (70.2 ± 13.4% at 10.5 months, positive correlation between body mass at 4 months and

1 3 866 Journal of Ornithology (2020) 161:859–871

Table 3 Age estimation of the Males Females Both males onset, culmination, completion, and females total duration and duration of the frst phase of voice breaking The onset of voice breaking (months) 7.7 ± 2.1 7.8 ± 1.6 7.7 ± 1.8 in Siberian Cranes (mean ± sd, (5.5–10.7) (6.8–9.6) (5.5–10.7) min–max and n) n = 7 n = 3 n = 10 The culmination of voice breaking (months) 9.4 ± 1.9 8.6 ± 1.5 9.2 ± 1.7 (6.5–12.3) (7.7–9.6) (6.5–12.3) n = 7 n = 2 n = 9 The completion of voice breaking (months) 11.6 ± 2.4 12.9 ± 0.3 12 ± 2 (7.4–12.8) (12.7–13.1) (7.4–13.1) n = 5 n = 2 n = 7 The duration of voice breaking (months) 5 ± 2.1 6 ± 0.1 5.3 ± 1.8 (1.9–7.3) (5.9–6.1) (1.9–7.3) n = 5 n = 2 n = 7 The duration of frst phase of voice breaking (months) 1.8 ± 1.5 1.7 ± 1.6 1.7 ± 1.5 (0.3–4.8) (0.9–2.8) (0.3–4.8) n = 7 n = 2 n = 9

duration of the frst phase of voice breaking (Table 2), but Table 4 Results of GLMM for separate and conjoint efects of indi- the relationship became insignifcant after sequential Bon- vidual and testosterone on the acoustic variables of chick’ voice breaking ferroni correction. However, we found signifcant correlation between the mean deltas of the high and low frequency Individual Testosterone Testosterone components between the closest recording sessions and tes- and individual tosterone level (for ΔMean_Perc_high: r = 0.29, p = 0.028, F F F for ΔMean_Perc_low: r = 0.32, p = 0.016; Spearman corre- 8,38 1,38 8,38 lation); these relationships also became insignifcant after Mean_Perc_f0 0.47 1.37 0.30 sequential Bonferroni correction. Similarly, GLMM showed ΔMean_Perc_f0 0.93 9.75* 1.44 a signifcant efect of “testosterone” for the mean deltas of Mean_Perc_g0 0.55 2.60 0.20 each of the components between the closest recording ses- ΔMean_Perc_g0 2.28* 18.96** 3.03** sions (ΔMean_Perc_f0 and ΔMean_Perc_g0) and a signif- **p < 0.001, *p < 0.05, ns—p > 0.05 cant efect of “individual” and of conjoint factor “individual with testosterone” for the mean delta of low-frequency component between the closest recording sessions (ΔMean_ Perc_g0; Table 4). A comparison of F-ratios showed that the efect of testosterone on voice-breaking variables was always Discussion stronger than the efect of the other factors (Table 4); these relationships remain signifcant after a sequential Bonferroni In our study we showed that the transition from the juve- correction (Table 4). nile to adult calls in Siberian Crane goes through the stage, Although we failed to find strong statistical relation when a call contains two independent fundamental fre- between voice breaking parameters and body mass in Sibe- quency components. Thus, Siberian Cranes, as at least four rian Cranes through the development, we noticed some tem- other crane species (Sandhill, Eurasian, Red-crowned and poral coincidence between them. Thus, the onset of voice Demoiselle Cranes: Niemeier 1979; Gebauer and Kaiser breaking immediately followed the end of active body mass 1998; Klenova et al. 2010, 2014), have a special period of gain that occurred at 7.5 months (Fig. 3b). At the same time, their life, the voice breaking, when they can produce such the age of culmination of voice breaking and signifcant calls with f0 and g0. We found that an average age of the changes in mean percentages of the high and low frequency onset and completion of Siberian Crane voice breaking is components showed an obvious relation to the change of 7.7 ± 1.8 and 12 ± 2 months respectively. Our sample did testosterone level, which increased signifcantly between not allow us to compare these parameters of voice break- 9.5 and 10.5 months of life on average (Fig. 3a, c). We also ing between sexes statistically, however, we did not notice observed this pattern at the individual level: for most chicks, any signs of sexual diferences in our study species, just signifcant changes in the mean percentages of the high and as other researchers had not found them previously in the low frequency components in calls occurred along with a other crane species (Sandhill, Red-crowned and Demoi- registered increase in testosterone levels (Fig. 4). selle Cranes: Niemeier 1979; Klenova et al. 2010, 2014).

1 3 Journal of Ornithology (2020) 161:859–871 867

Fig. 4 Changes from age to age in body mass (circles), testosterone level (triangles) and mean percentages of high f0 (rhom- buses) and low g0 (squares) fundamental frequency components in six examined Siberian Crane chicks

Comparing the ages of voice breaking completion in dif- sometimes feed their chicks from bill to bill and defend them ferent studied crane species, we can conclude that they are from other adult cranes (Archibald 1976; Johnsgard 1983; quite similar, in spite of large diferences in adult body size, Weekley 1985; Tacha 1988; Archibald and Meine 1996). age of the onset of voice breaking and completion of intense Our results are consistent with the hypothesis of prolonged body growth (Table 5; Klenova et al. 2010, 2014). The voice parental care as we showed for one more crane species, the breaking in all the species ends with the beginning of a new Siberian Crane, that the complete disappearance of juvenile breeding season at 10–12 months of life. Before the new fundamental frequency component from the calls occurs on breeding season, adult cranes cease taking care of young average soon after the start of the new breeding season and birds and start driving them away (Kamata 1994; Archibald the transition of young cranes to an independent life. and Lewis 1996). It was hypothesized earlier that the long If we compare the ages of voice breaking onset in difer- retention of the high-frequency juvenile calls of young birds ent crane species, we can see that they vary more between might induce parent behavior and decrease aggression of species than the ages of voice breaking completion do (from adults towards their chicks until the new breeding season 2 to 7.5 months of life; Table 5; Klenova et al. 2010, 2014). starts (Klenova et al. 2010, 2014). Despite the fact that We tried to fnd the possible triggers of the onset of voice crane chicks are precocial and are able to walk one day after breaking in Siberian Crane, but we did not observe a signif- hatching, they depend on their parents during all the frst cant correlation between it and body mass or testosterone year of their lives. Even in winter and early spring, parents level at diferent ages. In Demoiselle Crane the absence of

Table 5 Age estimation of the Demoiselle Crane Red-crowned Crane Siberian Crane onset, completion and total duration of voice breaking in Body mass of adults in autumn (kg) 2.6 ± 0.3 9.1 ± 0.8 6.8 ± 0.7 three studied crane species, n = 19 n = 10 n = 24 according to literature data Age of body mass gain completion (months) 2 7 7.5 (both males and females are included; mean ± sd and n are The onset of voice breaking (months) 2.3 ± 1.5 7.1 ± 2 7.7 ± 1.8 given) n = 14 n = 24 n = 10 The completion of voice breaking (months) ~ 10 11.6 ± 1.2 12 ± 2 n = 8 n = 24 n = 7 The duration of voice breaking (months) ~ 7.7 4.6 ± 2.1 5.3 ± 1.8 n = 8 n = 24 n = 7 References Klenova et al. (2014) Klenova et al. (2010) Present study

1 3 868 Journal of Ornithology (2020) 161:859–871 signifcant correlation between the onset of voice breaking (e.g. Goller and Larsen 1997; Fee et al. 1998; Mindlin and and hatching month, clutch order and body mass of a chick Laje 2005; Elemans et al. 2015). Since all of the studied at the age of 30, 40, 50 and 75 days was also found previ- Grus species start to produce low call frequencies at the age ously (Klenova et al. 2014). We can assume that the stated of 6–7 months (Niemeier 1979; Gebauer and Kaiser 1998; characteristics do not have a signifcant impact on the tim- Klenova et al. 2010; present study), we can guess that crane ing of the voice breaking in cranes. However, we can notice chicks use some tuning of the syringeal membranes to main- that the termination of body mass gain is immediately fol- tain the call frequency within a restricted frequency range. lowed by the onset of voice breaking in all studied crane Although the mechanisms for such tuning are still unclear, species (Table 5). Thus, the smallest crane of the world, the we propose that crane chicks may actively control elements Demoiselle Crane, stops its intense body mass gain at the of their vocal apparatus. For example, they might adjust the age of two months, and the heaviest crane of the world, the fundamental frequency of their calls by varying the length of Red-crowned Crane,—at seven months. At the same age, the vibrating portion of the syringeal membranes, the degree the frst signs of the beginning of a voice breaking appear in of their stretching, subsyringeal pressure, or include the dif- these species (Klenova et al. 2010, 2014). Siberian Cranes ferent layers of vibrating tissues to the vocalization process stop their intense body mass gain a little bit later than the as have been proved for some other bird species (e.g. Beck- Red-crowned Cranes, at the age of 7.5 months, although ers et al. 2003; Zollinger and Suthers 2004; Beckers and ten they are smaller in size. At the same age, Siberian Cranes Cate 2006; Zollinger et al. 2008; Elemans et al. 2015). Such also emit the frst calls with the low-frequency components a control could allow juveniles to override any direct rela- (g0; Table 4). So, we can suppose that the end of intense tionship between the full-growth syrinx size and unexpect- body growth might be a trigger for a beginning of a complex edly high frequency of calls. However, physiological experi- vocal reconstruction in cranes. Obviously, the plateauing of ments are necessary to fnd out how adolescent cranes can body growth is followed by a production of low fundamental produce such complex two-frequency vocalizations during frequency component (g0) in juvenile calls. the voice breaking and whether they do so with one or both It should be stated, however, that the body mass gain halves of the syrinx (e.g. Goller and Suthers 1996; Zollinger does not correspond to the end of body size growth, and Suthers 2004; Zollinger et al. 2008). which stops in Siberian Crane signifcantly earlier, at the Again, as it has been stated above, this prolonged reten- age of ~ 100–120 days, when the young cranes begin to tion of high-frequency juvenile call by young cranes may fy (Postelnykh and Kashentseva 2005). At the same age, serve for maintenance of prolonged parental care. Until large crane species from genus Grus fnish their tracheal acquiring the full body mass (that in genus Grus occurs in elongation and syrinx growth (Sandhill crane: Niemeier winter, at the age of 6–8 months), young cranes especially 1979; Red-crowned crane: Klenova et al. 2010). However, require parental care and protection. Maybe, they could the end of growth of the body size and the vocal apparatus actively control their syringeal membranes to emit high- does not correlate with the start of voice breaking, which frequency juvenile calls only to exaggerate their helpless- occurs much later both in Sandhill, Red-crowned and Sibe- ness. After the end of body mass growth the adolescents may rian cranes (Niemeier 1979; Klenova et al. 2010, Present weaken such kind of vocal tuning and their full-developed study). The birds’ vocal organ, syrinx, is known to be capa- vocal apparatus starts to produce low-frequency adult calls ble to produce complex vocal solutions even under simple as well. So, we can suppose that the end of intense body physiological motor commands (Fee 2002; Fee et al. 1998; mass gain may serve as a functional, rather than morphologi- Suthers and Margoliash 2002; Mindlin and Laje 2005). cal trigger for a beginning of a complex vocal restructuring The resulting fundamental frequency of signal and mode in cranes. of oscillation depend on internal mechanical properties of Although studies of vocal ontogenesis in other bird spe- sound-producing apparatus and its ability to operate with cies did not consider the relationship between the onset of diferent layers of vibrating tissues, rather than external voice breaking and the end of body mass gain, nevertheless, size and view of the organ (Titze 1994; Svec et al. 2000; we can assume its existence in some cases. Thus, in Aldabra Berry 2001; Elemans et al. 2015). Self-sustaining syringeal White-throated Rail (Dryolimnas cuvieri aldabranus) low- vocal membranes oscillations are supposed to be maintained frequency adult calls are frst heard from juveniles at the age through fuid-tissue interactions and myoelastic restoring of about 12 weeks, when they are almost reaching an adult forces generated within the tissues (Titze 1994; Titze and size (Wilkinson and Huxley 1978). The majority of chicks Alipour 2006), that prevent muscles from contractions at the of several seabird species, namely the Leach’s Storm-petrel rate of tissue vibration or other periodic input (Herbst et al. (Oceanodroma leucorhoa), Thin-billed Prion (Pachyptila 2012). So the discrepancy between the observed syrinx size belcheri), Crested Auklet (Aethia cristatella), Tufted and and the fundamental call frequencies is not so paradoxical Horned Pufns (Fratercula cirhata and F. corniculata), in the light of recent studies on the structure of this organ retain their high-frequency juvenile vocalizations at least

1 3 Journal of Ornithology (2020) 161:859–871 869 until fedging at ~ 35–45 days when they have almost full long time after the completion of voice breaking, which usu- size and weight (Naugler and Smith 1992; Duckworth et al. ally fnishes at the end of the frst year of their life (Niemeier 2009; Klenova and Kolesnikova 2013). But nevertheless, 1979; Klenova et al. 2010, 2014; present study). However, additional studies are necessary to fnd out how strong and detailed studies are still necessary to clarify the role of hor- widespread this relationship is. mones in vocal development of cranes. We can only suppose, In our study, we also tried to describe variation of tes- that in case of cranes testosterone afects both the behav- tosterone level in Siberian Cranes during the frst year of iour (e.g. Groothuis and Meeuwissen 1992; Goodship and their life in comparison with adolescent (18-month old) and Buchanan 2007), and the mechanisms of sound producing adult cranes (in condition at the end of the breeding season). in adolescents, e.g. via androgen receptors in the syringeal However, this description is very rough, since we measured structures (Godsave et al. 2002). Another possible explana- testosterone with a very low sampling rate, i.e. in large time tion is that testosterone somehow accelerates the develop- intervals, though the blood testosterone level could change ment of two-frequency calls into stereotyped adult-like ones considerably even during a single day (e.g. Kirkpatrick et al. (e.g. Harding 2004; Alliende et al. 2010). The full-fedged 1976; Rose et al. 1978; Plymate et al. 1989). So we could cranes who passed their frst winter, do not require parental miss a number of short testosterone pulses and the real care anymore in spring, but they need to establish them- impact of this hormone may be underestimated. selves in groups of adolescents in which young cranes spend Our sample did not allow us to compare the testoster- the 2nd–3rd years of life (Johnsgard 1983; Archibald and one values between sexes statistically; however, we did not Meine 1996). In such a situation, high-frequency juvenile notice any signs of sexual diferences in this parameter for calls, as well as the general chick-like behaviour become a the studied age period (Table 2). It is not surprising since, disadvantage, whereas the low-frequency adult calls together on the one hand, not only the testes, but also the ovaries and with more confdent and aggressive behaviour could help partly adrenals and perhaps even the brain may synthesize young cranes to occupy a good social position in groups of testosterone in birds and mammals (e.g. Longcope 1986; non-breeders (e.g. Fitch 1999). Burger 2002; Arnold 2004; Ketterson et al. 2005); on the Thus, in this study we showed that Siberian Crane chicks other hand, outside the breeding season the testosterone level possess the voice breaking. It starts in Siberian Crane, as may not show sex diferences at all (e.g. Kellam et al. 2004; well as in Red-crowned and Demoiselle Cranes (Klenova Ketterson et al. 2005). Then, we found that testosterone level et al. 2010, 2014), when chicks slow down their body did not vary signifcantly between most ages, but showed growth, and ends with the beginning of a new breeding an evident rise in spring, at the age of 10.5 months. At this season. The culmination of voice breaking occurs together age, the culmination of voice breaking in Siberian Crane with a signifcant increase of testosterone level in spring. also happened (Fig. 3b). However, we did not test the other We suggest that voice breaking of cranes is triggered by the cranes species in our lab, with our protocol, so the compari- end of chicks’ body growth, is stimulated by the increase of son of our results with those of other research groups may be testosterone levels, and ends after adult cranes stop taking invalid because each lab uses diferent protocols, for exam- care of their chicks. ple, diferent antibodies/kits with diferent cross-reactivity. Similar to cranes, sudden development of vocal character- Acknowledgements We thank Elina Antonyuk, Svetlana Bobkova, Fulica ameri- Tatiana and Kirill Postelnykh, Anna Sudakova and Galina Nosachenko istics was also observed for American Coot ( for their help with data gathering and Elena Mudrik for the help with cana) (Cosens 1981) and Green Woodhoopoe (Phoeniculus PCR DNA sexing analysis. During our work, we adhered to the “Guide- purpureus) (Radford 2004). The voice breaking in these lines for the treatment of animals in behavioural research and teaching” species fnishes with maturation, which is determined as a (Anim. Behav. 65: 249–255) and to the laws of Russian Federation, the country where the research was conducted. This study was funded development of sexual ornamentation (Cosens 1981; Rad- by the Russian Foundation for Basic Research (Grant 12-04-00414). ford 2004). Some other studies also have demonstrated that the call development of non-oscines can be hormonally infu- enced (e.g. Groothuis and Meeuwissen 1992; Fusani et al. 1994). It has been well demonstrated that steroid hormones References could also afect syrinx development (e.g. Wolf and Wolf 1951; Takahashi and Noumura, 1987; Veney and Wade 2005 Adret P (2012) Call development in captive-reared Pied Avocets, Recurvirostra avosetta. J Ornithol 153:535–546 etc), neural control centers (e.g. Schlinger 1998; Wade and Alliende JA, Méndez JV, Goller F, Mindlin GB (2010) Hormonal accel- Buhlman 2000; Wade et al. 2002) and motor control mecha- eration of song development illuminates motor control mechanism nisms in birds (e.g. Alliende et al. 2010). In cranes, the voice in canaries. Dev Neurobiol 70:943–960 breaking and sexual maturation are separated with a long Archibald GW (1976) The unison call of cranes as a useful taxonomic tool. Dissertation, Cornell University period of time: sexual maturation comes only on second- Archibald GW, Lewis JC (1996) Crane biology. In: Ellis D, Gee third year of their life (Archibald and Meine 1996), that is a G, Mirande C (eds) Cranes: their biology, husbandry, and

1 3 870 Journal of Ornithology (2020) 161:859–871

conservation. National Biological Service and International Crane Gebauer A, Kaiser M (1998) Anmerkungen zur Lautenwicklung und Foundation, Baraboo (WI), pp 1–30 zum Stimmbruch beim Grauen Kranich (Grus grus). Brandenbur- Archibald GW, Meine CD (1996) Family gruidae (Cranes). In: del gische Umwelt Berichte 3:25–33 Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the Godsave SF, Lohmann R, Vloet RPM, Gahr M (2002) Androgen recep- world, vol 3. Hoatzin to Auks Lynx Edicions, Barcelona, pp 60–89 tors in the embryonic zebra fnch hindbrain suggest a function Arnold AP (2004) Sex chromosomes and brain gender. Nat Rev Neu- for maternal androgens in perihatching survival. J Comp Neurol rosci 5:701–708 453:57–70 Baker MC, Baker MS, Gammon DE (2003) Vocal ontogeny of nest- Goller F, Suthers RA (1996) Role of syringeal muscles in gating air- ling and fedgling Black-Capped Chickadees Poecile atricapilla fow and sound production in singing brown thrashers. J Neuro- in natural populations. Bioacoustics 13(3):265–296 physiol 75:867–876 Beckers GJL, Suthers RA, ten Cate C (2003) Mechanisms of fre- Goller F, Larsen ON (1997) A new mechanism of sound generation in quency and amplitude modulation in ring dove song. J Exp Biol songbirds. Proc Natl Acad Sci 94:14787–14791 206:1833–1843 Goodship NM, Buchanan KL (2007) Nestling testosterone controls Beckers JL, ten Cate C (2006) Nonlinear phenomena and song evolu- begging behaviour in the pied fycatcher Fidecula hypoleuca. tion in Streptopelia doves. Acta Zool Sin 52:482–485 Horm Behav 52:454–460 Berry DA (2001) Mechanisms of modal and nonmodal phonation. J Grifths R, Double MC, Orr K, Dawson R (1998) A DNA test to sex Phon 29:431–450 most birds. Mol Ecol 7:1071–1075 Bragina E (2004) A case of premature breaking of voice in a chick of Groothuis T, Meeuwissen G (1992) The infuence of testosterone on the Siberian crane Grus leucogeranus (Gruidae, Aves). Abstracts the development and fxation of the form of displays in two age of 10th International Behavioral Ecology Congress; Jyväskylä, classes of young black-headed gulls. Anim Behav 43:189–208 Finland, p 28 Harding CF (2004) Hormonal modulation of singing, hormonal modu- Bragina EV, Beme IR (2007) The sexual and individual diferences in lation of the songbird brain and singing behaviour. Ann NY Acad the vocal repertoire of adult Siberian Cranes (Grus leucogeranus, Sci 1016:524–539 Gruidae). Zoologicheskii Zhurnal 86:1468–1481 Heinroth O (1927) Die Vögel Mitteleuropas. Bd. III, Berlin (Nachdruck Budde C (1999a) The vocal repertoire of the Grey Crowned Crane 1968) Balearica regulorum gibbericeps. I: the tonal and the non-har- Herbst CT, Stoeger AS, Frey R, Lohscheller J, Titze IR, Gumpen- monic calls. Bioacoustics 10:161–173 berger M, Fitch WT (2012) How low can you go? Physical pro- Budde C (1999b) The vocal repertoire of the Grey Crowned Crane duction mechanism of elephant infrasonic vocalizations. Science Balearica regulorum gibbericeps. II: the unison call. Bioacoustics 337:595–599 10:191–201 Hudiakova TA (2002) Early development of acoustical communica- Budde C (2001) Ontogeny of calls of a nonpasserine species: the Grey tion in Siberian Crane (Grus leucogeranus) chicks. M.S. Thesis, Crowned Crane Balearica regulorum gibbericeps. Afr J Ecol Lomonosov Moscow State University (in Russian) 39:33–37 Johnsgard PA (1983) The Cranes of the world. Indiana University Burger HG (2002) Androgen production in women. Fertil Steril Press, Bloomington 77(Suppl 4):S3–S5 Kamata M (1994) Family breakup of the Red-crowned Crane Grus Catchpole CK, Slater PJB (2008) Bird song: biological themes and japonensis at an artifcial feeding site in eastern Hokkaido, Japan. variations. Cambridge Univ Press, Cambridge In: Higuchi H, Minton J, Kurosawa R (eds) The future of Cranes Cosens SE (1981) Development of vocalizations in the American Coot. and wetlands. Proceedings of the International Symposium. Wild Can J Zool 59:1921–1928 Bird Society of Japan, Tokyo, pp 149–155 Dragonetti M, Caccamo C, Corsi F, Farsi F, Giovacchini P, Pollonara Kellam JS, Wingfeld JC, Lucas JR (2004) Nonbreeding season pair- E, Giunchi D (2013) The vocal repertoire of the Eurasian Stone- ing behavior and the annual cycle of testosterone in male and curlew (Burhinus oedicnemus). Wilson J Ornithol 125(1):34–49 female downy woodpeckers, Picoides pubescens. Horm Behav Duckworth A, Masello JF, Mundry R, Quillfeldt P (2009) Functional 46:703–714 characterization of begging calls in Thin-billed Prions Pachyptila Ketterson ED, Nolan V Jr, Sandell M (2005) Testosterone in females: belcheri chicks. Acta Ornithol 44:127–137 mediator of adaptive traits, constraint on sexual dimorphism, or Engländer W, Bergmann H (1990) Sex specifc voice development in both? Am Nat 166:S85–S98 the Shelduck Tadorna tadorna. J Ornithol 131:174–176 Kirkpatrick JF, Vail R, Devous S, Schwend S, Baker CB, Wiesner L Elemans CPH, Rasmussen JH, Herbst CT, Düring DN, Zollinger SA, (1976) Diurnal variation of plasma testosterone in wild stallions. Brumm H, Srivastava K, Svane N, Ding M, Larsen ON, Sober SJ, Biol Reprod 15:98–101 Švec JG (2015) Universal mechanisms of sound production and Klenova AV, Kolesnikova YA (2013) Evidence for a non-gradual pat- control in birds and mammals. Nat Commun 6:8978 tern of call development in Auks (Alcidae, Charadriiformes). J Fee MS (2002) Measurement of the linear and nonlinear mechanical Ornith 154:705–716 properties of the oscine syrinx: implications for function. J Comp Klenova AV, Volodin IA, Volodina EV (2007) The vocal develop- Physiol A 188:829–839 ment of the Red-crowned Crane Grus japonensis. Ornithol Sci Fee MS, Shraiman B, Pesaran B, Mitra PP (1998) The role of nonlinear 6:107–119 dynamics of the syrinx in the vocalizations of a songbird. Nature Klenova AV, Volodin IA, Volodina EV, Postelnykh KA (2010) Voice 395:67–71 breaking in adolescent Red-crowned Cranes (Grus japonenis). Fitch W (1999) Acoustic exaggeration of size in birds via tracheal Behaviour 147:505–524 elongation: comparative and theoretical analyses. J Zool Lond Klenova AV, Goncharova MV, Bragina EV, Kashentseva TA (2014) 248:31–48 Vocal development and voice breaking in Demoiselle Cranes Fusani L, Beani L, Dessi Fulghieri F (1994) Testosterone afects the (Anthropoides virgo). Bioacoustics 23(3):247–265 acoustic structure of the male call in the grey partridge (Perdix Li F, Wu JD, Harris J, Burnham J (2012) Number and distribution of perdix). Behaviour 128:301–310 cranes wintering at Poyang Lake, China during 2011–2012. Chin Garskaia MA, Chernyi AG (1979) Analysis of vocal development and Birds 3:180–190 vocal production in Japanese Quail. Ornithology 14:62–76 (in Longcope C (1986) Adrenal and gonadal androgen secretion in normal Russian) females. Clin in Endocrinol Metab 15:213–228

1 3 Journal of Ornithology (2020) 161:859–871 871

Marchenko AA, Beme IR, Sarychev EI (2018) Ontogeny of vocaliza- Suthers RA, Margoliash D (2002) Motor control of birdsong. Curr tion in diurnal birds of prey (Falco cherrug, Accipiter gentilis). Opin Neurobiol 12:684–690 Zoologicheskii Zhurnal 97(6):712–722 Tacha TC (1988) Social organization of Sandhill Cranes from mid- Marler P, Slabbekoorn H (2008) Nature’s music. The science of bird- continental North America. Wildl Monogr 99:1–37 song. Elsevier, Academic Press, Amsterdam Takahashi MM, Noumura T (1987) Sexually dimorphic and laterally Marques PAM, de Araujo CB, Vicente L (2010) Nestling call modi- asymmetric development of the embryonic duck syrinx: efect of fcation during early development in a colonial passerine. Bio- estrogen on in vitro cell proliferation and chondrogenesis. Dev acoustics 20:45–58 Biol 121:417–422 Meinert U, Bergmann H (1983) Zur Jugendentwicklung der Lautäu- ten Thoren B, Bergmann H (1986) Veränderung und Konstanz von ßerungen beim Birkhuhn (Tetrao tetrix). Behaviour 85:242–259 Merkmalen in der jugendlichen Stimmentwicklung der Nonnen- Mindlin GB, Laje R (2005) The physics of birdsong. Springer Verlag, gans (Branta leucopsis). Behaviour 100:61–91 Berlin ten Thoren B, Bergmann H (1987) Die Entwicklung der Lautäußerun- Moran MD (2003) Arguments for rejecting the sequential Bonferroni gen bei der Graugans (Anser anser). J Ornithol 128:181–207 in ecological studies. Oikos 100:403–405 Titze IR (1994) Principles of voice production. Englewood Clifs, Naugler C, Smith P (1992) Vocalizations of nestling Leach’s Storm- Prentice Hall, NJ petrels. Condor 94:1002–1006 Titze IR, Alipour F (2006) The myoelastic aerodynamic theory of pho- Niemeier M (1979) Structural and functional aspects of vocal ontogeny nation. National Center for Voice and Speech, Denver CO in Grus canadensis (Gruidae: Aves). Ph. D. thesis, University of Veney SL, Wade J (2005) Post-hatching syrinx development in the Nebraska, Lincoln zebra fnch: an analysis of androgen receptor, aromatase, estrogen Olsen GH, Carpenter JW, Langenberg JA (1996) Medicine and sur- receptor α and estrogen receptor β mRNAs. J Comp Physiol A gery. In: Ellis D, Gee G, Mirande C (eds) Cranes: their biology, 191:97–104 husbandry, and conservation. National Biological Service and Wade J, Buhlman L (2000) Lateralization and efects of adult androgen International Crane Foundation, Baraboo (WI), pp 137–174 in a sexually dimorphic neuromuscular system controlling song in Plymate SR, Tenover JS, Bremner WJ (1989) Circadian variation in zebra fnches. J Comp Neurol 426:154–164 testosterone, sex hormone-binding globulin, and calculated non- Wade J, Buhlman L, Swender D (2002) Post-hatching hormonal modu- sex hormone-binding globulin bound testosterone in healthy lation of a sexually dimorphic neuromuscular system controlling young and elderly men. J Androl 10:366–371 song in zebra fnches. Brain Res 929:191–201 Postelnykh KA, Kashentseva TA (2005) Development of Siberian Weekley FL (1985) Individual and regional variation in calls of the crane. In: Vinter S, Ilyashenko E (eds) Cranes of eurasia, Vol 2. Greater Sandhill Crane. M.S. Thesis, University of Wisconsin Moscow, pp 240–254 (in Russian) Wilkinson R, Huxley CR (1978) Vocalizations of chicks and juveniles Radford A (2004) Voice breaking in males results in sexual dimor- and the development of adult calls in the Aldabra White-throated phism of Green Woodhoopoe calls. Behaviour 141:555–569 Rail Dryolimnas cuvieri aldabranus (Aves: Rallidae). J Zool Lond Redondo T (1991) Early stages of vocal ontogeny in the Magpie (Pica 186:487–505 pica). J Ornith 132:145–163 Wolf E, Wolf E (1951) The efects of castration on bird embryos. J Rice WR (1989) Analyzing tables of statistical tests. Evolution Exp Zool 116:59–97 43:223–225 Würdinger I (1970) Erzeugung, Ontogenie und Funktion der Lautäu- Riska DE (1986) An analysis of vocal communication in young Brown ßerungen bei vier Gänsearten (Anser indicus, A. caerulescens, A. Noddies (Anous stolidus). Auk 103:351–358 albifrons und Branta canadensis). Z Tierpsychol 27(3):257–302 Rose RM, Gordon TP, Bernstein S (1978) Diurnal variation in plasma Zollinger SA, Suthers RA (2004) Motor mechanisms of a vocal mimic: testosterone and cortisol in rhesus monkeys living in social implications for birdsong production. Proc R Soc Lond B Biol groups. J Endocrinol 76:67–74 Sci 271:483–491 Schlinger BA (1998) Sexual diferentiation of avian brain and behavior: Zollinger SA, Riede T, Suthers RA (2008) Two-voice complexity from current views on gonadal hormone-dependent and independent a single side of the syrinx in northern mockingbird Mimus poly- mechanisms. Annu Rev Physiol 60:407–429 glottos vocalizations. J Exp Biol 211:1978–1991 Smallwood JA, Dudajek V (2003) Vocal development in American kestrel (Falco sparverius) nestlings. J Raptor Res 37(1):37–43 Publisher’s Note Springer Nature remains neutral with regard to Svec JG, Horácek J, Sram F, Veselý J (2000) Resonance proper- jurisdictional claims in published maps and institutional afliations. ties of the vocal folds: in vivo laryngoscopic investigation of the externally excited laryngeal vibrations. J Acoust Soc Am 108:1397–1407

1 3