(2021) 12:10
Meshcheryagina and Opaev ﻿Avian Res
https://doi.org/10.1186/s40657-021-00246-9

Avian Research
Open Access

RESEARCH

Previously unknown behavior in parasitic
cuckoo females: male‑like vocalization
during migratory activity
Swetlana G. Meshcheryagina1*

and Alexey Opaev2

Abstract
Background: In the last decade, enigmatic male-like cuckoo calls have been reported several times in East Asia.
These calls exhibited a combination of vocal traits of both Oriental Cuckoo (Cuculus optatus) and Common Cuckoo(Cuculus canorus) advertising calls, and some authors therefore suggested that the enigmatic calls were produced byeither Common × Oriental Cuckoo male hybrids or Common Cuckoo males having a gene mutation. However, theexact identity of calling birds are still unknown.
Methods: We recorded previously unknown male-like calls from three captive Oriental Cuckoo females, and compared these calls with enigmatic vocalizations recorded in the wild as well as with advertising vocalizations of Common and Oriental Cuckoo males. To achieve this, we measured calls automatically. Besides, we video-recorded captive
female emitting male-like calls, and compared these recordings with the YouTube recordings of calling males of both
Common and Oriental Cuckoos to get insight into the mechanism of call production.
Results: The analysis showed that female male-like calls recorded in captivity were similar to enigmatic calls
recorded in the wild. Therefore, Oriental Cuckoo females might produce the latter calls. Two features of these female
calls appeared to be unusual among birds. First, females produced male-like calls at the time of spring and autumn
migratory activity and on migration in the wild. Because of this, functional significance of this call remained puzzling.
Secondly, the male-like female call unexpectedly combined features of both closed-mouth (closed beak and simultaneous inflation of the ‘throat sac’) and open-mouth (prominent harmonic spectrum and the maximum neck extension observed at the beginning of a sound) vocal behaviors.
Conclusions: The Cuculus vocalizations outside the reproductive season remain poorly understood. Here, we found
for the first time that Oriental Cuckoo females can produce male-like calls in that time. Because of its rarity, this callmight be an atavism. Indeed, female male-like vocalizations are still known in non-parasitic tropical and apparently
more basal cuckoos only. Therefore, our findings may shed light on the evolution of vocal communication in avian
brood parasites.
Keywords: Closed-mouth vocal behavior, Cuckoo call, Cuculus optatus, Female song, Male-like vocalization*Correspondence: meshcheryagina_sg@ipae.uran.ru
1
Institute of Plant and Animal Ecology, Ural Branch of the Russian
Academy of Sciences, Ekaterinburg, Russia
Full list of author information is available at the end of the article

BackgroundIn cuckoos, vocal data are widely used to resolve the taxonomy and for species identification (Payne 2005). For
example, Oriental Cuckoo (Cuculus optatus) and Himalayan Cuckoo (Cuculus saturatus) are often regarded as
separate species, because the advertising calls of the twodiffer in the presence/absence of introductory note and© The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing,
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Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

the number of notes (King 2005; Payne 2005; Lindholmand Linden 2007; Xia et al. 2016). In the last decade, enigmatic cuckoo calls have been reported in eastern Asia: inSouth Korea (Moores 2013,2015) and in Primorski Kraiof Russian Far East (Lastukhin 2015; own data SM). The
photos of three calling bird have been taken. On thesephotos, however, traits necessary for exact species and/or
sex identification were poorly seen (Moores 2015).
It was noticed that the enigmatic calls exhibited a combination of vocal traits of both Oriental Cuckoo andCommon Cuckoo (Cuculus canorus). Based on this, Lastukhin (2015) suggested that Common × Oriental Cuckoo
hybrids might produce these calls. Indeed, calls and songs
can be intermediate in hybrid individuals due to genetical or cultural transmission or both (Payne 1980; Cadena
et al. 2007; Marova et al. 2017). In parasitic cuckoos, however, hybrids are still unknown (Payne 2005; McCarthy2006). The absence of hybridization in parasitic cuckoos
could be at least partly due to their innate stereotypicalsounds preventing mistakes in mate recognition (Lack
1968; Graves 1992; Payne 2005). Other authors who
reviewed the existing evidence of birds’ hybridization in
Russia Far East, also doubted about the cuckoos’ hybridization (Gluschenko and Korobov 2016; Gluschenko
et al. 2016). Concerning South Korean recordings, Clive
F. Mann, who is one of the authors of the book Cuckoosof the World (Erritzøe et al. 2012), assumed that the calls
were produced by Common Cuckoo having a gene mutation (Moores 2013). Other authors, however, argued that
enigmatic calls apparently were not caused by a single
rare mutation, as they have been recorded and/or heard
several times (Gluschenko et al. 2016).
All the aforementioned authors suggested that cuckoo
males produced enigmatic calls. Indeed, the most commonly heard female call, that is, the bubbling call (Payne
2005; Erritzøe et al. 2012), differs considerably from boththe male call and enigmatic call. In Cuculus, bubbling
calls differ among species in time and frequency parameters, and in the number of notes, although overall structures are similar with each other (Kim et al. 2017b). There
are also other call types in female repertoires. However,their structure and functional significance are poorly
understood (Cramp 1985). By contrast, the advertising‘cu-coo’ call of Common Cuckoo male is especially wellstudied (Fuisz and De Kort 2007; Jung et al. 2014; Weiet al. 2015; Kim et al. 2017a; Li et al. 2017; Moskát et al.
2017, 2018; Zsebök et al. 2017; Benedetti et al. 2018; Tryjanowski et al. 2018; Deng et al. 2019a; Xia et al. 2019),
including its rare aberrant version ‘cu-kee’ (Møller et al.
2016; Moskát et al. 2021). It is well known, however, thatfemale birds can produce song and/or male-like advertising vocalization in several species (Odom et al. 2014;
Boeme and Goretskaia 2016), including non-parasitic

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tropical cuckoos (Brumm and Goymann 2017), and duetsand chorus are especially characteristic for such species(Tobias et al. 2016). Besides, in some species females havebeen found to sing when the male disappeared or when
the testosterone level experimentally enhanced (Garamszegi et al. 2007).
In this study, we recorded captive Oriental Cuckoo
females and compared their calls with enigmatic vocalizations, and with typical advertising calls of both Common and Oriental Cuckoos. We found that the enigmaticcalls were produced by Oriental Cuckoo females during
migratory activity. Thus, it appeared to be unusual interms of its functional significance.
A striking feature of adult male of several cuckoo species is the concentration of its acoustic energy into a
low frequency. In birds, low-frequency sound is usuallyfavored by closed-mouth vocal behavior due to the resonance condition generated by that behavior (Riede et al.
2016). Apart from a few exceptions, closed-mouth vocalization is employed by advertising males. The usage ofthis behavior by female birds is poorly studied. Male-likefemale cuckoo call is rather low-frequency sound. Therefore, we additionally analyzed the possible mechanismsof call production by female, and then compared themwith those of males.

Methods
Data on individuals that produced the enigmatic callsin the wild and in captivity

In the wild, the enigmatic calls were reported 22 times,
in eastern Asia only (Fig. 1a; Table 1). In the majority (13out of 22) of the aforementioned cases, the calling individual had not been seen. In the one case, both Common Cuckoo and Oriental Cuckoo (grey morph) wereobserved in the locality, where the enigmatic calls were
just heard. In five cases, it was possible just to understood that the calling bird was cuckoo. Photos and videorecording of three calling individuals have been taken on
Baekryeong Island. Back view as well as distance to photographer and optical effects prevent exact species identification in these cases (Moores 2015).
In total, from 2011 onwards, we held in captivity six
Oriental Cuckoo females at different times, but up to
three females simultaneously. Three (F1, F2 and F3) out
of six females produced male-like vocalizations that
resembled closely the enigmatic cuckoo calls. All females
held in a single heated room (15 m­ 2) having the window on the south side and artificial UV-light in winter.
They lived in group and moved freely around the room.
There were many perches in the room used by cuckoos. The room connected to the loggia (7.5 ­m2), wherefemales spent a time readily during spring and summer
months. This room simultaneously acts as an office forMeshcheryagina and Opaev ﻿Avian Res(2021) 12:10

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Fig. 1 Localities of origin of captive females and where analyzed recordings were obtained in the wild. a The localities of origin of captive females
are shown by red circles, while other circles show localities in which the enigmatic vocalizations were either recorded (black circles) or just reporter(grey circles) in the wild. b Studied Oriental Cuckoo females in captivity (photos were taken during the molt). Abbreviations: F1, F2, F3, Oriental
Cuckoo females from Khakassia (Kh), Krasnoyarsk Krai (Kr) and Ekaterinburg (Sv), respectively; Pr, recording locality of “Common × Oriental Cuckoo
hybrid” in Primorski Krai; Ko, recording locality of “unknown cuckoo” in South Korea; Hb, recording locality of “atypical song of Oriental Cuckoo” in
Hebei, China; Tw, recording locality of “atypical song of Oriental Cuckoo” in Taiwan, China (see Additional file 1: Table S1 for details)

Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

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Table 1 Atypical cuckoo calls reported (recorded) from the wild
Location

Coordinates

Year

Number of registrations

Recorded/reported by

43.37°N, 132.57°E

2008

1

A. Khodakov, personalcommunication, 12.05.
2019

Primorski Krai of Russian Federation
Shkotovsky District

Hasansky District

42.48°N, 130.66°E

2015

3

own data SM

Chernigovsky District

44.38°N, 132.80°E

2015

2

Lastukhin (2015)34.07°N, 125.11°E

2000
2009

1
1

Moores (2013)

The South Korean Yellow Sea Islands
Gageo-do Island
Eocheong Island

36.12°N, 125.97°E

2003 or 2004

1

Moores (2013)

Baekryeong Island

37.94°N, 124.66°E

2013
2014
2015

3
4
3

Moores (2013)
Moores (2015)
Moores (2015)

Weiyeon Island

36.22°N, 126.08°E

2014

1

Moores (2015)

China
Hebei Province

39.14°N, 118.83°E

2005

1

Mathias Ritschard, XC21559

Wusatou, Kinmen, Taiwan

24.47°N, 118.29°E

2020

1

Ting-Wei, Hung, XC559436

the researcher. Diet of females consisted of insects andprotein substitutes.
Female F1 originated from the nest of Western Greenish Warbler (Phylloscopus (trochiloides) viridanus) foundin Khakassia (Khakassia Nature Reserve, Maly Abakan:
52.059°N, 89.597°E, Fig. 1a). This female was taken fromthe nest at the age of 15 days on 12 July, 2019. Female
F2 was mist-netted as adult in Krasnoyarsk Krai (Enisei
Ecological station ‘Mirnoe’ of Severtsov Institute of Ecology and Evolution: 62.289°N, 88.977°E, Fig. 1a) on 25
June, 2016. Female F3 was found as adult in Ekaterinburg(56.815°N, 60.537°E, Fig. 1a) on 3 June, 2017. This female
was injured at that time. Female F1 was grey morphhaving rufous fringes of the feathers of the breast, andfemales F2 and F3 were rufous morph (Fig. 1b). All threefemales emitted bubbling calls that only female cuckoos
produce. Besides, female F2 laid an egg in captivity.
Collecting calls

Along with male-like vocalization of Oriental Cuckoo
females (n = 3 individuals) and enigmatic atypical cuckoo
calls recorded in the wild (n = 4 individuals), for comparison we analyzed also advertising calls of males of Oriental (n = 10 individuals) and Common (n = 10 individuals)
Cuckoos. In total, recordings of 27 individuals were studied, and recordings of 26 of them were used in statistical analysis. For all but one individual, we analyzed 10
two-note calls per individual (only 5 atypical calls wererecorded for one individual): i.e. totally 255 calls in 26
individuals.
Three Oriental Cuckoo females were recorded in captivity. Among these individuals, only two were used in

the statistical analysis (see below). In the analysis, we also
used four enigmatic recordings of atypical cuckoo calls(Additional file 1: Table S1). Some of these recordings
were previously classified as either ‘unknown cuckoo’(recorded in South Korea; Additional file 1: Table S1) or‘Common × Oriental Cuckoo hybrid’ (Lastukhin 2015;
recorded in Primorski Krai of Russian Federation; Additional file 1: Table S1).
Most of the recordings of typical male advertisement
call of both Common (n = 10 males) and Oriental (n = 10)
Cuckoos were downloaded from Xeno-canto (xenocanto.org) except two recordings made by AO in Khingan
State Nature Reserve (Amur Region of Russian Federation) in 2017 and 2018 (Additional file 1: Table S1). The
geographic variation of advertisement call parameters
had been found at least in Common Cuckoo (Wei et al.
2015). Therefore, for the analysis we chose the recordings obtained in eastern Asia (Additional file 1: Table S1)
to allow the correct comparison with the recordings ofatypical cuckoo calls also obtained in this region.
Call analysis

Following standard terminology, a ‘note’ is defined as thesmallest building block visible as a continuous line on aspectrogram (Catchpole and Slater 2008). In Common
and Oriental Cuckoo males, a single call (e.g. the wellknown ‘cu-coo’ of Common Cuckoo) usually but notalways consists of two notes (Xia et al. 2016; Moskát et al.
2017, 2018; Benedetti et al. 2018; Tryjanowski et al. 2018;
Deng et al. 2019a). Only two-note calls were characteristic for three out of four analyzed recordings of enigmatic
atypical vocalization (Fig. 2d–f ), while one individualMeshcheryagina and Opaev ﻿Avian Res(2021) 12:10

began to vocalize with three-note calls but switchedthen to two-note calls (Fig. 2g). For Oriental Cuckoo
females, however, it was typical to alternate single-note,
two-note and three-note male-like calls in a sequence(Fig. 2a, b). In the statistical analysis, we used two-note
female calls only in order to compare them with otherrecordings. Only two out of three females were includedin this analysis because the recordings of the third individual consisted mostly from single-note calls, and only
three two-note calls were recorded from this female.

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Nevertheless, females’ single-note and three-note calls
considered below briefly.
Besides, we described briefly the syntax of male-likeand atypical call sequences. To do so, we analyzed 39
uninterrupted call sequences of females F1–F3, and six
atypical call sequences recorded in the wild (four audioand two video-recordings; the latter were not included in
the call analysis mentioned above).
Sonograms were produced using Syrinx PC v. 2.6(John Burt, www.syrin​xpc.com) with an FFT size = 512,and a window type = Hanning. First of all, we allocatedFig. 2 Spectrograms of male-like a–c and atypical d–g vocalizations. The figure shows vocalization of a female F1 Oriental Cuckoo, b female F2
Oriental Cuckoo, c female F3 Oriental Cuckoo, d “unknown cuckoo” from South Korea, e “Common × Oriental Cuckoo hybrid” from Primorski Krai
(Russia), as well as f two atypical calls recorded in Taiwan (China) and g atypical call recorded in Hebei Province (China). For A-notes (i.e. notes ofboth male-like and atypical calls), the numbers highlight position of note in the call (e.g. A2 means the second A-note). Variants of male-like andatypical calls: A1, single-note calls, A1–A2, two-note calls, and A1–A2–A3, three-note call. B, Kuk-call; INT, introductory call. Calls separated by dottedlines are from the same individual; all others are from different individuals

Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

each note of each call in a single wav file. The subsequent analysis was done in R software (R Core Team).
We used ‘autodetect’ function in warbleR package in R
(Araya-Salas and Smith-Vidaurre 2017) to detect signal (i.e. note) within each wav file across the frequency
range of 0–5 kHz using threshold of 5%. We then used
‘specan’ function (frequency range 0–5 kHz, threshold5%) in warbleR package in R to automatically measure 21
acoustic parameters (listed in Additional file 2: Table S2)of each note of two-note call across all analyzed wav files(i.e. 42 parameters for each two-note call; Additional
file 3: Table S3).
Analysis of video‑recordings

To get insights into the mechanisms of call production,
we video-recorded female F1 Oriental Cuckoo during
emitting of either male-like vocalization (eight recordings) or bubbling call (one recording) using action camera Sony FDR-AS3000 with remote control. Female
was recorded with a speed of 60 frame/s, from 8 to 20
February, 2020. Totally, we analyzed nine recordingsof X ± SE = 0.9 ± 0.5 min each (8.1 min in total), andthese recordings were not used in the acoustic analysis described above. Brief inspection of the recordings
revealed that female emitted the male-like call with theclosed beak and inflated neck. It is well known that suchfeatures are characteristic for so-called ‘closed-mouth
vocalization’, that is, the vocal behavior with the closed
beak and simultaneous inflation of the esophagus ortracheal pouches; closed-mouth vocal behavior generally favors low-frequency sounds (Fletcher et al. 2004;
Riede et al. 2004, 2016). Therefore, while analyzing videorecordings of female F1, we looked for the compliance
between the bird posture and the produced sound bycomparing the screenshots of a video-recording with thecorresponding time points in the spectrogram. Totally,
we analyzed in such a way seven notes from three different calls of female F1. We aimed to estimate the amountof the extension of the neck region. To do so, we selected
six manually placed points in each successive video frameof each note. We then estimated the area of polygon
between these points (in pixels) using Adobe Photoshop
21.1. The minimal value of this measurement of note, thatwas measured either immediately before or just after that
note, was considered as 100% (separately for each note).
Then, the area of the neck region in each video frame ofnote was estimated relative to this minimal value. We
then compared the median relative volume of the neckregion during the first and second parts of each note. To
do so, we compared three screenshots that corresponded
to the first half of a note with three screenshots from thesecond half.

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The data on female F1 Oriental Cuckoo were then compared with the video-recordings of calling males of thefour Palearctic cuckoo species: Oriental Cuckoo (recordings of n = 21 of individuals), Common Cuckoo (n = 24),
Indian Cuckoo (C. micropterus; n = 13), and Lesser
Cuckoo (C. poliocephalus; n = 22). The video-recordingsof these individuals were downloaded from YouTube(Additional file 4: Table S4).
Statistical analysis

In order to assess and visualize difference/similarity in
two-note calls of the analyzed individuals in the multivariate acoustic space, we ran a principal component
analysis (PCA) using factorextra package in R (Kassambara and Mundt 2017). In the analysis, we used measurements of each parameter of both first and second notesof a two-note call (i.e. 21 × 2 = 42 parameters per eachcall). Before the PCA was ran, we used REdaS package in
R (Hatzinger et al. 2014; Maier 2015) to evaluate whether
our data were suitable for this analysis. We found ourdata suitable, because Bartlett’s test of sphericity showedthat the correlation matrix was significantly different
2 = 41,365.2,
from an identity matrix (Chi-square test: χ861
P < 0.0001), and the Kaiser–Meyer–Olkin measure ofsampling adequacy was 0.82 (above the minimum acceptable value of 0.5; Kaiser 1974) indicating that a large proportion of variance in the variables can be explained by
the components.
Two-sample Student t-tests were used to test differences between four groups: (1) Common Cuckoo males,(2) Oriental Cuckoo males, (3) two captive females, and(4) four individuals that produced atypical calls in thewild. Additionally, in the analysis of video-recordings weused dependent two-group Wilcoxon Signed Rank test in
R software.

Results
When and on what circumstances was male‑like
vocalization reported in captivity and in the wild

In captivity, we recorded male-like vocalization of
females at the time of spring and autumn migratory
activity (Fig. 3). This activity lasted ca. 2–2.5 months anddisplayed the cyclic pattern: a 5–10-day period of nightly
activity alternated with a 1–7-day period of nightly
inactivity. The exact dates of migratory activity and its
duration differed among the three females. By contrast,
bubbling call produced almost year-round several (upto three) times per week, but the most often during thebreeding season (i.e. in May–July: up to several times perday; Additional file 5: Movie S1).
At nights, females emitted bubbling call only (Fig. 4b).
By contrast, male-like vocalization (Fig. 4a) producedin either morning (6:00 a.m.–01:00 p.m.) or evening

Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

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Fig. 3 Annual dynamic of male-like vocalization of females Oriental Cuckoo in captivity. Yellow color corresponds to female F1, red to F2, and black
to F3. The numbers inside squares indicate a date when an individual called (dates when a given individual called in different years are marked withasterisks)Fig. 4 Daily dynamic of calls of Oriental Cuckoo females in captivity. a Male-like calls, b Babbling calls. Yellow color corresponds to female F1, red toF2, and black to F3(03:20–09:50 p.m.) hours, and much rarely in the night(10:00 p.m.–01:00 a.m.). While emitting male-like vocalization, females used the only perch in 60–70% of observations. This perch was lit by rising or setting sun, andthe sky was readily seen from the perch (Additional file 6:
Movie S2). Females other than calling one did not show
any changes in behavior while the male-like vocalization
was produced.
In the wild, the enigmatic atypical cuckoo calls havebeen mostly reported in May, that is, during spring
migration. In Taiwan, China, calls were recorded on

18 May (Kinmen 2020). In South Korean Islands, theearliest date was 9 May (Gageo-do Island, 2000), andthe latest dates were 25 May (Gageo-do Island, 2009)
and 26–28 May (Baekryeong Island, 2013 and 2014)(Moores 2013, 2015). The dates for Primorski Krai of
Russian Federation were: 17 May and 19 May, 2015 in
Chernigovsky District (Lastukhin 2015), 30 May and
1–2 June, 2015 in Hasansky District (own data of SM),and 8 July, 2008 (recorded by A. Khodakov). In the wild,
the atypical cuckoo calls were reported between 7:30
and 10:40 a.m. (n = 3).

Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

Structure and organization of female male‑like callsequences

Females emitted three variants of male-like call having
either one, two or three notes (variants A1–A3; Fig. 2a–c;
Additional file 7: Audio S1). It was typical to alternate
these call variants in a single sequence, and most longcall sequences contained both three-, two- and singlenote call variants. In females F1, F2 and F3, the length ofrecorded male-like call sequences varied from 8 to 93 s
(mean ± SD = 56.1 ± 22.4 s, n = 39), and the number ofcalls in sequence was from 4 to 79 (mean ± SD = 45 ± 19,
n = 39).
Two main syntactic features were characteristic formale-like call sequences of females (Additional file 8: Figure S1). Firstly, females usually called with eventual variety, where every call variant occurred in a bout consistingof several repetitions of the same variant. Secondly, typically there were more notes in calls produced in the
beginning of a sequence rather than in calls emitted at
the end of that sequence.
Two other call types can be rarely found in boutsof male-like vocalization. The first was Kuk-call (after
Cramp 1985; call type B in Fig. 2a–c) that appeared to be
more typical for among-individual communication during feeding or resting, when another female flew closely
to the calling one (own observation in captivity). The
second was the introductory call consisted of 4–7 broadband notes (Fig. 2a). In female F1 sequences began oftenwith an introductory call (Additional file 8: Figure S1).
Besides, four additional short acoustic sequences (thesesequences not shown in Additional file 8: Figure S1) consisted from either the only introductory call or the introductory call followed by 1–2 male-like calls.
The length of atypical cuckoo call sequences recorded in
the wild varied from 5 to 60 s (mean ± SD = 31.3 ± 23.0 s,
n = 6), and the number of calls in sequence was from 5 to
43 (mean ± SD = 23 ± 17, n = 6). It seemed possible, thatat least some of these recordings were not made fromthe very beginning of call sequence. All but one of thesesequences consisted from two-note calls only. In one
recording, cuckoo began calling with three-note calls,
and then switched to two-notes calls.

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correlation with PC2: peakedness of the spectrum andasymmetry of the spectrum of both notes A1 and A2, andmodulation index of note A2.
The PCA clearly separated the analyzed individuals
into three groups. The first two groups were males of
either Common or Oriental Cuckoos. The third group
included both two captive females and four individuals that produced atypical call in the wild (Fig. 5). We
thus hypothesized that atypical cuckoo calls might havebeen produced by females (presumably Oriental Cuckoo
females because the male-like call is unknown in wellstudied Common Cuckoo).
These three groups appeared for us to differ clearlyaurally. Two frequency characteristics of both female
male-like call and atypical call seemed to best distinguishthem from advertising call of males of both Common andOriental Cuckoos. First, they located in higher frequency
ranges: e.g. both notes had the highest values of third
quartile and maximum dominant frequencies (Additional
file 3: Table S3). Secondly, the fundamental frequency ofthese calls covered the wider range that was expressed ine.g. the highest values of interquartile frequency range
and modulation index of the first note (Additional file 3:
Table S3).
Besides, in males of both Common and Oriental Cuckoos, the majority of energy was in fundamental frequency
and there was little detectable energy in higher harmonics. By contrasts, both female and atypical calls haveprominent harmonics along with fundamental frequency(Fig. 2).
Motor patterns of calling in Oriental Cuckoo female

While producing male-like call, female Oriental Cuckoo
adopted a striking posture slightly leaning forward andstretching the neck, beak closed and the ventral and dorsal neck regions considerably inflated (Additional file 8:

Acoustic characteristics of calls

In this section, we considered two-notes calls only. Using
PCA, we extracted the first two PCs (eigenvalues 1.7 and
3.9, respectively). PC1 explained 81.6% of the total variation, and PC2 explained a cumulative 99.0%. Peakednessof the spectrum of the first note, as well as peakednessof the spectrum and asymmetry of the spectrum of thesecond note showed the highest absolute correlation
with PC1. The following parameter showed the strongest

Fig. 5 PCA of 42 acoustic parameters of two-note calls of four groups
of individuals

Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

Figure S2). The enlargement of the neck regions was
obviously produced by airflow through the syrinx in the
expiratory direction while the beak was closed. It was
unexpected, however, that the dorsal neck region inflated
more than the ventral region (Additional file 8: FigureS2b). In other respects, the posture of calling female did
not have any specific features: as usually, female sat on abranch in a vertical position, wing tips laying on top of
the tail, head slightly raised, and neck extended. Besides,
at each note, the wings threw up pressing against thebody.
The analysis of video-recordings revealed that the
inflation of the neck region, assessed by its relative area,
began to increase some 1–3 ms before the note arestarted to produce. The median of maximum increase
was 118% (range 110–126%, n = 7 notes) relative to minimal volume (100%) of the neck region between calls. The

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neck region did not completely collapse between the successive notes of a call (3 in Fig. 6b).
We compared the median relative volume of the neckregion during the first and second parts of a note. We
found that the volume during the first half of a note
exceeded that of the second half (dependent two-group
Wilcoxon Signed Rank test: V = 28, n = 7, P = 0.022). The
median difference between median relative volume of thefirst and second halves of a note was 3%, range 1–6% (themedian volume of the neck region during the first halfof a note exceeded that of the second half in all analyzed
notes). Therefore, at the beginning of each note the neckregion attained the maximum volume, and then generally
decreased towards the end of the note (the middle notein Fig. 6b, c is a bright example).
While producing bubbling and introductory calls,
female did not adopt any specific posture. She did not

Fig. 6 Changes in the amount of neck region inflation while emitting male-like call. The figure illustrated a sequence of three notes of three-note
male-like call of female F1. The amount of inflation was estimated by measuring the area of the neck region as indicate by red dotted lines a; theenlargement of the neck region was estimated as the percentages relative to minimal inflation, i.e. before and/or after calling b. Three notes areshown spectrographically in the bottom panel cMeshcheryagina and Opaev ﻿Avian Res(2021) 12:10

inflate the neck region, and widely open the beak during
calling (data not shown; Additional file 5: Movie S1).
Motor patterns of calling in males of the four Palearctic
cuckoo species

Males of all species lower their wing tips below the taillevel while producing advertising call (Additional file 8:
Figure S3). This is the only feature of the calling posturesof both Indian and Lesser Cuckoos, the later sometimes
also leaning forward. It should be noted that Lesser
Cuckoo produces calling not only from a perch, but often
also in flight (Panov 1973; own observations in Primorski
Krai of Russia, and in Hunan Province of China). Whilecalling, both Indian and Lesser Cuckoos widely open thebeak, while only slightly inflating the throat.
The most peculiar posture is characteristic for Common Cuckoo male. Male of this species lifts the tail up,
spreads the tail feathers, and swings tail from side to side.
While sitting on a steady perch (e.g. on a thick branchor a stone), male can prominently lean forward until
the body took almost horizontal orientation (Additional
file 8: Figure S3). Each call of a male consists of two different notes (Fig. 7g), and the motor pattern differs between
the first and second note of a call. The first, more highpitched note coincides with the slight opening of thebeak, and the neck stretching; the ventral and dorsal neckregions (‘throat sac’) inflates moderately (Fig. 7e). Whenthe second note produces, the beak closed, the ‘throatsac’ inflated prominently, the head slightly leaned down,
and the neck shortened (Fig. 7f ).
The large ‘throat sac’ (i.e. both ventral and dorsal neckregions) extension is characteristic for the productionof both (apparently identical) notes of Oriental Cuckoo
call. The beak closes during call production (Fig. 7b) andopens slightly only immediately before calling (Fig. 7a).
While calling, male bended the back becoming ‘roundshouldered’, shortened the neck, and sometimes alsoslightly raised the tail showing the undertail-coverts.
Before emitting a note, male slightly raised his head, andthen lowered it down simultaneously with calling.

Discussion
The origin of enigmatic male‑like cuckoo calls: from whom
and when?

Recently, cuckoo calls exhibited a combination of vocal
traits of both Oriental Cuckoo and Common Cuckoothat were reported from East Asia (Moores 2013, 2015;
Lastukhin 2015; own data SM). The calling individual was
not identified exactly in any report because either thebirds keep shy or automated audio recorders were used
for call recording. The author who took photos of three
calling individuals was not able to identify the species
exactly (Moores 2015).

Page 10 of 16

Here, we found that the enigmatic male-like calls
recorded in the wild might have been produced byfemales (most probably—Oriental Cuckoo females). We
concluded this based on the PCA analysis of 42 automatically measured acoustic parameters of cuckoo calls. The
analysis showed that PC1 and PC2 coordinates clearlyplaced the two groups of individuals among each other’s:
the first group consisted of individuals that produced
enigmatic atypical calls in the wild, and the second groupconsisted of captive Oriental Cuckoo females that produced male-like calls. Both atypical and male-like calls
have detectable energy in higher harmonics. By contrast,
aberrant cuckoo calls (that were not considered in thispaper) apparently lack higher harmonics in both Common (see Fig. 1 in Moskát et al. 2021) and Oriental (seerecording of SM at Xeno-canto.org: XC609612) Cuckoos.
In captivity, Oriental Cuckoo females produced singleand three-note males-like calls along with two-note calls.
In the wild, two- and three-note atypical male-like calls
were recorded. In two- and three-note calls, either the
first note (in two-notes call) or both the first and second
notes (in three-note call) usually were more high-pitched(Additional file 3: Table S3) and louder. The same pattern
have been found in ‘cu-coo’ and ‘cu-cu-coo’ calls of Common Cuckoo male (Payne 2005; Erritzøe et al. 2012). In
this species, two- and three-note calls have been found touse in different context, and the ‘cu‐cu‐coo’ calls are associated with females emitting their bubbling call (Xia et al.
2019).
In the wild, male-like vocalization have been only
rarely reported, and only three out of six captive females
produced this type of vocalization. Therefore, probably
not all females emitted this call. However, the rarity ofreports of the male-like call in the wild could be also dueto the overall shyness of comparatively badly studied Oriental Cuckoo as compared to Common Cuckoo (Cramp
1985; Payne 2005; Erritzøe et al. 2012).
Our data suggested that one more reason could
explain the rarity of female male-like vocalization. We
supposed that females produce male-like call during
migration only. The vocal behavior of parasitic cuckoos is almost completely unknown in this time (Cramp
1985; Payne 2005; Erritzøe et al. 2012). Several facts
were in favor of our point of view. Firstly, we reported
vocalization of captive females during their migratory
activity only, starting from the age of several months,
that is, from the age of the first migration. Secondly, thelocations from which enigmatic calls were reported in
the wild are located in a strip stretching from south tonorth along the coast of eastern Asia (Fig. 1a), that is,on the typical migration route of cuckoos. Thirdly, thecalls were reported from the wild mostly in May, i.e. at
the time of spring migration (in East China and RussianMeshcheryagina and Opaev ﻿Avian Res(2021) 12:10

Page 11 of 16

Fig. 7 The screenshots of calling postures of males of Oriental a–c and Common d–f Cuckoos. The spectrograms of calls are shown in the bottom
panel (g, x-axis = time in s; y-axis = frequency in kHz), and the lowercase letters over blue arrows indicate the time position of corresponding
still-frame images a–f. Common Cuckoo male produces the first note of a call with the open beak e, and the second note is produced while thebeak is closed f. By contrast, Oriental Cuckoo male produces both notes with the closed beak b, and the beak is opening slightly only just before
calling a. The enlargement of throat is characteristic for calling in both species (red arrows), and is the most apparent when the beak is closed. The
video-recordings used for the analysis were downloaded from https​://www.youtu​be.com/watch​?v=4rq4J​8i9QN​o (Oriental Cuckoo) and https​://www.youtu​be.com/watch​?time_conti​nue=11&v=wejl6​ukN8y​c&featu​re=emb_logo (Common Cuckoo)

Far East, the Oriental Cuckoo migration occurs frommiddle April until late May (La Touche 1931–1934;
Gluschenko et al. 2016). Fourthly, Oriental Cuckoo is aregular migrant but probably does not breed on South
Korean Island Baekryeong from which enigmatic calls

were reported (Moores 2007, 2013). Fifthly, the obviously migrating bird was observed calling in Hasansky
District by the authors. Within three days, this individual stayed in a broken oak forest where leaf-warblers(host species) do not breed.

Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

We do not know yet, however, can females of other
Cuculus species produce male-like call? If the answer
will be ‘yes’, then do the calls of different species differ?
For instance, female bubbling call differs among species
in frequency and number of notes (Kim et al. 2017b),
although overall structures are similar with each other(Payne 2005; Erritzøe et al. 2012).
Towards the mechanisms of call production in maleand female cuckoos

During calling, Oriental Cuckoo male closes the beakand prominently inflates the throat. Common cuckoo
male does the same while emitting the second note of its‘cu-coo’ call, but the first note produces with the slightly
opened beak and only moderately inflated throat. Probably, esophagus inflation is the most likely mechanism thatcauses the throat (‘throat sac’) extension during callingin both cuckoos, as it was suggested or proved for Pectoral Sandpiper (Calidris melanotos) (Riede et al. 2015),
Ring Dove (Streptopelia risorii) (Riede et al. 2004), andWhite-browed Coucal (Centropus superciliosus) (Brumm
and Goymann 2017). However, other mechanisms, e.g.
the inflation of the tracheal or gular vocal sacs (reviewed
in Dantzker 2015) are possible. The closed beak during
calling allows for the inflation of the esophagus (and/or
associated vocal sacs), and means that the bird vocalizes
into the closed, inflated cavity with the sound radiating
through the skin of the neck.
The low fundamental frequency and absence of higher
harmonics are characteristic for the advertising call ofmales of both Common and Oriental Cuckoos. Moreover, the frequency seemed to depend on the motor pattern. For example, both notes of Oriental Cuckoo callhave the lowest peak frequency (mean 0.46 kHz; Additional file 3: Table S3), and males of this species appeared
to inflate the throat the most. While emitting the second
note of a call (mean peak frequency = 0.66 kHz; Additional file 3: Table S3), Common Cuckoo males also
prominently inflate the throat (cf. Fig. 7b, f ). At last, thefirst note of a call of Common Cuckoo that produces withthe slightly open beak had the highest peak frequency(mean 0.81 kHz; Additional file 3: Table S3).
It is well known that all the aforementioned features(except that of the first note of Common Cuckoo call) are
the most important characteristics of the closed-mouth
vocalization: (1) low fundamental frequency, (2) absenceof higher harmonics, (3) inflation of the ‘throat sac’, and(4) closed beak (Fletcher et al. 2004; Riede et al. 2004,
2016). We thus conclude that both the advertisement
call of Oriental Cuckoo and the second note of Common

Page 12 of 16

Cuckoo call appear to be true closed-mouth vocalizations. By contrast, advertising vocalization of both Indianand Lesser Cuckoos is open-mouth as the beak widely
opens while calling.
At the first glance, male-like call of Oriental Cuckoo
female was apparently the closed-mouth vocalization
as well. Indeed, this sound was prominently lower thanthe much more typical for female bubbling call. In Common Cuckoo, bubbling call had frequency between 1 and2.5 kHz (Deng et al. 2019b; Moskát and Hauber 2019),
and in Oriental Cuckoo the corresponding values were
1.2 and 2.3 kHz (Kim et al. 2017b). By contrast, male-likecall had the peak frequency below 1 kHz (means of thefirst and second notes were 0.82 and 0.74 kHz, respectively; Additional file 3: Table S3). The peculiar calling
posture of Oriental Cuckoo female with inflated neck andclosed beak that we describe in this study could play arole in lowering the voice of female, as it was found for
closed-mouth vocalizations in other species.
Two features of female male-like call, however, contradicted treating of this call as the true closed-mouth
vocalization. Firstly, male-like call had the prominent
spectrum as the higher harmonics were readily seen on
the spectrograms (Figs. 2a–g, 6c). By contrast, the typicalclosed-mouth vocalization had only one major resonancefrequency, that is, the fundamental frequency of the signal. The absence of higher harmonics may result from thelow-pass filter characteristic of the esophagus wall andoverlying skin (Fletcher et al. 2004).
Secondly, as birds typically (but not exclusively) vocalize during expiration (Wild et al. 1998), in closed-mouth
vocalization maximum inflation occurs at the end of thesound because the enlargement of the ‘throat sac’ is produced by airflow through the syrinx in the expiratory
direction while the beak and nares are closed (Riede et al.
2004). By contrast, in female Oriental Cuckoo maximum
neck extension was observed at the beginning of a note,and the amount of neck inflation generally decreased
towards the end of the note (Fig. 6b). This pattern is characteristic for open-mouth vocal behavior. For example, in
Radde’s Warbler (Phylloscopus schwarzi, an open-mouth
singer) at the beginning of each song syllable the ‘throatsac’ attains the maximum volume, while at the end ofeach song syllable the ‘throat sac’ volume reduces to minimal value (Opaev and Shishkina 2020).
Therefore, unlike male advertising call, male-like callof female may not be typical closed-mouth vocalization in Oriental Cuckoo. It might be that the latter callproduces without complete rerouting of the air into an
inflatable structure (e.g. with a narrow beak gape and/or open nares). The vocalizations with an almost closed

Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

beak are well known in birds (Reichard and Welkin 2015),
but should be treated as open-mouth vocalization (Riedeet al. 2016). Nevertheless, the Oriental Cuckoo female
vocalization appeared to be rather unusual among birds
as it combined features of both closed-mouth (almostor completely closed beak, inflated neck region, and low
frequency of the sound) and open-mouth (prominent
harmonic spectrum and the pattern of dynamic of theamount of neck extension during calling) vocalizations.
It should be noted that during calling the dorsal neckregion of female inflated more than the ventral neckregion (Additional file 8: Figure S2b). Similarly, in malesof both Common and Oriental Cuckoos the dorsal neckregion inflated noticeably (Fig. 7b, f ). It seems unusual,
because in birds the dorsal neck region typically does notextend during vocalization. We do not know yet whatparticular structure has inflated in the dorsal part of theneck of Oriental Cuckoo female.
Functional significance of cuckoo calls

The possible functional significance of female male-like
vocalization is puzzling. To date, only two cuckoo calls
have been studied in details: male advertising call andfemale bubbling call. Both call types are used during thebreeding season and have multiple functions. We consider these functions below in order to hypothesize what
the possible function of female male-like call might be.
First of all, male advertising call and female bubbling call are used in spacing behavior. In the breeding
grounds, both males and females have home ranges ofroughly similar sizes that are defended to some extent
from same-sex rivals (Nakamura and Miyazawa 1997;
Honza et al. 2002; Vogl et al. 2004; Nakamura et al. 2005;
Payne 2005; Erritzøe et al. 2012; Williams et al. 2016;
Moskát and Hauber 2019; Moskát et al. 2019; Yun et al.
2019). To repel same-sex rivals, males use advertisingcall (Moskát et al. 2017, 2018; Tryjanowski et al. 2018)
while females emit bubbling call (Davies 2015; Moskát
and Hauber 2019). In females, aggression towards otherfemales appear to be important as they compete strongly
for the nests of host-species (Nakamura and Miyazawa
1997; but see Vogl et al. 2004). We suppose that malelike call does not play a role in spacing behavior as it did
not use during breeding season when home ranges aremonopolized most.
Cuckoos might also use their calls to communicate
individuality. Indeed, advertising calls of males have beenfound to differ among individuals (Jung et al. 2014; Liet al. 2017; Zsebök et al. 2017). However, within-season
consistency of individually distinctive vocal characteristics appeared to be small (Deng et al. 2019a), and this call

Page 13 of 16

is thus unlikely to reveal certain individual. Bubbling calls
also vary greatly in each individual (Deng et al. 2019b).
Similarly, it seems unlikely that females use male-likecalls for individual recognition. The latter vocalization
was very rare, found in only a fraction of individuals, anddid not use in the breeding season when individual recognition appeared to be the most important.
It is generally assumed that male cuckoos use advertising call for mate attraction (Payne 2005). However, recently it was found that females did not exhibit
response to playback of both typical and aberrant malecalls (Xia et al. 2019; Moskát et al. 2021). Similarly, malelike call did not elicit female response in captivity (owndata of SM). By contrast, the strong response to female
bubbling call has been found both in males (Kim et al.
2017b; Lee et al. 2019; Moskát and Hauber 2019; Xiaet al. 2019) and females (Lee et al. 2019; Moskát and Hauber 2019), including captive females (own data of SM).
Because males are usually attracted to advertising callsof unfamiliar individuals (Moskát et al. 2017, 2018), one
can assume that they would respond to female male-like
vocalization as well.
Probably, the vocalization could facilitate either prebreeding intersexual interactions or resting group gathering at stopover sites. Although cuckoos usually encounter
alone on migration, it is known that they can migrate
in loose groups, and sometimes also forage in groups in
wintering grounds and at stopover sites (Cramp 1985;
Payne 2005; Erritzøe et al. 2012).
Recently, it was found that both male and female
cuckoo calls influence both current host species (Yorkand Davies 2017) and rare suitable and unsuitable hosts(e.g. swallows, starlings, thrushes and some corvids;
Lyon and Gilbert 2013; Tryjanowski et al. 2018). A group
mobbing is normally observed in the presence of calling cuckoo. It should be noted that some host species
are able to distinguish between Common Cuckoo and a
predator (e.g. Sparrowhawk Accipiter nisus) because theiracoustic responses and behaviors differ depending on thepresence of either species (Welbergen and Davies 2008;
Yu et al. 2017a, b, 2019, 2020). The mobbing, in turn,can be useful for cuckoos, making it easier to find hostnests (Marton et al. 2019). We do not know yet whether
host species react to cuckoo outside the breeding season. However, it seems unlikely that the mobbing has any
functional significance for cuckoos in this time.

Conclusions
Our results might be interesting from the evolutionary
point of view as well. We found that Oriental Cuckoo
females can produce male-like calls outside the reproductive season. It might be that male-like vocal behavior

Meshcheryagina and Opaev ﻿Avian Res(2021) 12:10

has not any function. It is possible that the male-like calling could be just a seasonal manifestation of the female
singing lost in the evolution from non-parasitic to parasitic cuckoos. Female singing and duetting are indeed
found in several non-parasitic cuckoo species (Tobias
et al. 2016; Brumm and Goymann 2017).

Supplementary Information
The online version contains supplementary material available at https​://doi.
org/10.1186/s4065​7-021-00246​-9.
Additional file 1: Table S1. Recordings of analyzed individuals, including
source of recordings and origin of females recorded in captivity.
Additional file 2: Table S2. List of acoustic parameters (21) measured by
specan function of warbleR package and used to compare call structure.
Additional file 3: Table S3. Univariate statistics for measurements of twonotes calls of Oriental Cuckoo (OC) and Common Cuckoo (CC).
Additional file 4: Table S4. YouTube video-recordings of males of four
Cuculus species used in the analysis.

Page 14 of 16

Declarations
Ethical approval and consent to participate
All applicable international, national, and institutional guidelines for the careand use of animals were followed. This is an observational study. All work complied in accordance with the Federal law of Russian Federation No. 498-Ф3 ‘On
responsible treatment of animals’. The Research Bioethics Committee of theInstitute of Plant and Animal Ecology has confirmed that no ethical approvalis required.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests. The funders had
no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Author details
1
Institute of Plant and Animal Ecology, Ural Branch of the Russian Academyof Sciences, Ekaterinburg, Russia. 2 A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia.
Received: 24 September 2020 Accepted: 24 February 2021

Additional file 5: Movie S1. Female F1 emitting bubbling call during
migratory activity (Video-recording 13 July 2020, 11:17 p.m.).
Additional file 6: Movie S2. Female F1 emitting male-like calls (Videorecording 20 February 2020, 08:57 a.m.)
Additional file 7: Audio S1. Male-like calls of Female F2 (Audio-recording
15 February 2020, 00:21 p.m.)
Additional file 8: Figure S1. Schematic representation of 39 uninterrupted male-like call sequences of three Oriental Cuckoo females recodedin captivity, and of 6 atypical call sequences (all produced by different individuals) recorded in the wild. Figure S2. Calling females Oriental Cuckoo.
Figure S3. The screenshots of calling postures of cuckoo males.
Acknowledgements
The authors thank A.A. Meshcheryagin for his help in recording of captive
females; Y.N. Gluschenko, S.G. Surmach and G.N. Bachurin for their development of interest to enigmatic cuckoo vocalization and for informing theauthors about reports of such vocalization in Russian Far East; O.V. Bourski and
M.S. Galisheva for providing cuckoos to be held in captivity; A.A. Lastukhin forproviding cuckoo recording; authors who uploaded their audio- and videorecordings of cuckoos to Internet collections and made them freely available.
Authors’ contributions
SM recorded cuckoo calls in captivity and collected information about atypical
cuckoo vocalization in the wild, AO carried out the analysis, SM and AO wrote
the manuscript. Both authors have read and approved the final manuscript.
Funding
This study was performed within the frameworks of state contract with theInstitute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences (project number 18-9-4-22), and as a part of Program of the Russian
Academy of Sciences 2013–2020, No. AAAA-A18-118042690110-1 [0109-20190003] ‘Ecological and evolutionary aspects of animal behavior and communication’. Call analysis was supported by the Russian Science Foundation (grant
number 20-14-00058).
Availability of data and materials
The datasets supporting the conclusions of this article are included within thearticle and its additional files. Examples of male-like vocalization and bubbling
call of Oriental Cuckoo females are available at Xeno-canto (F1: XC624308,
XC624310, XC624312, XC624316, XC624322; F2: XC624326, XC624329,
XC624365; F3: XC624337, XC624350, XC624361). Other audio/video recordings
used in the study are available from the corresponding author on reasonable
request.

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