Ecological Indicators 66 (2016) 592–597

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

The number of syllables in Chernobyl cuckoo calls reliably indicate
habitat, soil and radiation levels
Anders Pape Møller a,∗ , Federico Morelli b , Timothy A. Mousseau c , Piotr Tryjanowski daEcologie Systématique Evolution, Université Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, F-91405 Orsay Cedex, France
Czech University of Life Sciences Prague, Faculty of Environmental Sciences, Department of Applied Geoinformatics and Spatial Planning, Kamýcká 129,
CZ-165 00 Prague 6, Czech Republicc
Department of Biological Sciences, University of South Carolina, SC 29208, USAdInstitute of Zoology, Poznań University of Life Sciences, Wojska Polskiego 71C, PL-60-625 Poznan, Polandb

a r t i c l e

i n f oArticle history:
Received 16 September 2015
Received in revised form 4 February 2016
Accepted 11 February 2016
Keywords:
Advertisement calls
Chernobyl
CuckooCuculus canorus
Habitat quality
Radioactivity
Species richnessa b s t r a c t
Cuckoos Cuculus canorus produce calls that consist of a repeated but variable number of syllables thathas given name to the species and the family. Here we tested the hypothesis that cuckoo calls are reliable indicators of environmental and individual quality by determining the number of repeated ‘cuckoo’syllables in calls in relation to habitat and soil, ionizing radiation, presence of a female cuckoo and local
density of male cuckoos at Chernobyl, Ukraine. Males were consistent in their production of syllables,
producing more syllables per call when a female or another male arrived. This increase in the number ofsyllables was larger in males that already produced many syllables in the absence of conspeciﬁcs, implying that males of superior quality were still able to increase the number of syllables. Males produced moresyllables per call in habitats with black soil and in forests. Furthermore, they produced fewer and moreaberrant syllables in radioactively contaminated areas of Chernobyl providing evidence of an effect ofenvironmental perturbation on the number of syllables. These ﬁndings are consistent with the hypothesis that the number of syllables is a condition-dependent signal used for attracting mates, repellingcompetitors, providing information about local environmental conditions for other cuckoos, but also forhumans and thus can be used by humans to infer habitat quality.
© 2016 Elsevier Ltd. All rights reserved.

1. Introduction
Parasitic cuckoos are highly vocal with their calls having givenrise to their name across numerous languages (Davies, 2015). Yet
there are hardly any studies of the function of their cuckoo calls.
Why should cuckoos produce so many and such loud calls, and what
do these calls signal to conspeciﬁcs and heterospeciﬁcs including
humans? Cuckoos are renowned for their obligate parasitic behavior, relying on hosts for rearing their offspring (Wyllie, 1981; Davies,
2000, 2015; Payne, 2005). Cuckoos have recently been shown tobe reliable indicators of biodiversity because their presence mirrors the species richness of their hosts and hence the overall bird
community (Morelli et al., 2015; Tryjanowski and Morelli, 2015).
Given that the Web of Knowledge had no less than 2181 publications on cuckoos on 31 July 2015 there is a surprising lack ofpublished information on the calls that have given name to thespecies and this bird family. Cuckoos are non-passerines that do not∗ Corresponding author. Tel.: +33 1 69 15 56 88; fax: +33 1 69 15 56 96.
E-mail address: anders.moller@u-psud.fr (A.P. Møller).
http://dx.doi.org/10.1016/j.ecolind.2016.02.037
1470-160X/© 2016 Elsevier Ltd. All rights reserved.

learn calls, but presumably have calls that are affected by inherent
genetic factors (Marler and Slabbekoorn, 2004). Hence, the expression of calls should be affected by mutations. Three studies haveinvestigated variation in spectral and temporal properties of cuckoo
calls. Fuisz and de Kort (2007) showed that call structures differed signiﬁcantly among male cuckoos occupying different typesof habitats. This observation combined with habitat imprinting
could provide a mechanism for maintenance of host speciﬁc cuckoo
races. Furthermore, Jung et al. (2014) showed that male cuckoos differed individually in the structure of their calls. Finally, Wei et al.
(2015) showed that the structure of the different components ofthe cuckoo call differed geographically and among subspecies.
The function of cuckoo calls is only poorly known. Cramp andPerrins (1986) termed the repeated cu-cooo syllable of this vocalization an advertisement call. Typically, a cuckoo call consists ofa sequence of repeated cu-coo sounds (each considered a syllable here) ending with a pause of a few seconds, the equivalent of
more than the duration of one syllable, which separates two different series of syllables. Up to 300 syllables have been reported
in a sequence. More rapid calls are given when a male is excitedwith a maximum of 26 syllables per 30 s (Bögershausen, 1976)

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delivered from a perch or rarely in ﬂight. Calls are given duringday, but also at night (Löhrl, 1950). Calls are produced throughout the breeding season, but at the beginning and the end calls arehoarse. Wyllie (1981) reported variation in the seasonal frequency
of calling although no details were reported. Calls are given muchless frequently in cold and thundery weather than when it is sunny(Groebbels, 1957; Melde, 1982).
Given the time and the effort used by cuckoos to produce
hundreds of calls daily, and given that calls can be heard at a distance of 2–3 km in calm weather depending on the habitat, thissuggests that cuckoo calls have an important signaling function. The
number of syllables produced by individual males in the hoopoe
Upupa epops (Martín-Vivaldi et al., 1998) and several passerines(Catchpole and Slater, 2008) are also consistent over time, suggesting a signaling function of call length. Previous studies have shownthat this call attribute predicts mating and reproductive success interms of extra-pair offspring in these species (Martín-Vivaldi et al.,1999, 2002; Catchpole and Slater, 2008). This raises the possibility
that similar mechanisms may be involved in vocal communicationin cuckoos as in other species of birds.
Cuckoos are unlikely to be distributed randomly because individual condition (and therefore call length) will be linked to habitat
quality and thus soil type. Soil may in turn affect plant coverand hence availability of insect food such as the abundance ofcaterpillar larvae that constitute the main source of nutrition for
cuckoos. Since larvae are located near the top of the soil, wheremost radionuclides are located, we might expect fewer caterpillars
and hence fewer butterﬂies in areas with higher background radiation level (Møller and Mousseau, 2009). Thus, there should be a
reduction in food abundance in more contaminated areas. Thesearguments suggest why the number of syllables in a cuckoo call isa reliable indicator of environmental conditions.
The objectives of this study were to assess the use of cuckoo calls
as indicators of environmental conditions. Speciﬁcally, we tested(1) whether the number of syllables was repeatable among calls of
an individual cuckoo; (2) whether more syllables were produced in
the presence of more conspeciﬁc males and females, and whether
this increase in the number of syllables with the appearance of aconspeciﬁc male or female was larger for males that initially had
many syllables. Such an increase in the number of syllables in maleswith initially many syllables is predicted by the handicap principle
and condition-dependent signaling. According to that hypothesis
signallers with an initially high level of signaling are also those thatare differentially able to signal at a higher level when challenged bya conspeciﬁc male or female (Zahavi, 1975; Johnstone, 1995); and(3) whether the number of syllables was a reliable indicator of environmental conditions as reﬂected by soil (clay, sand or black soil),habitat (forest or agricultural habitats) and radioactive contamination. We hypothesize that higher quality soils and more diverse
habitats would hold more caterpillars that are the preferred dietof the cuckoo (Cramp and Perrins, 1986) and therefore would holdcuckoos in better condition. We test explicitly whether the abundance of butterﬂies varies among soil types differing in abundanceof cuckoos.

2. Methods
2.1. Study sites
APM studied cuckoos in Ukraine in forested areas of a total of2000 km2 in the Chernobyl Exclusion Zone and outside this area
ranging from Bobor, Dytiatki and Pisky to Ivankov with a small
control area around Voronkov. This study lasted 27 May – 10 June2015 and was part of an extensive bird census program consistingof point counts covering a total of 250 census points each lasting593

5 min (see Møller et al. (2015) for further details). APM and TAM
also recorded cuckoos with aberrant call that deviated from ordinary cuckoo syllables during extensive ﬁeldwork in the Chernobyl
Exclusion Zone 1991–2014.
2.2. Recording the number of syllables
We recorded the number of syllables (each syllable being a single cu-coo) that a cuckoo male produced in a single call by waiting
for a call to be ﬁnished in order to avoid inclusion of calls that were
initiated before arrival of the observer. Once the male started to singagain, we recorded the number of syllables in the next two calls, if
possible (some males left before a second call was initiated). This
allowed for repeatability analysis of the number of syllables per callbased on the second and the third call. A call was considered to beﬁnished when at least a period of time similar to that of a syllable
had passed without a new syllable being produced.
If a female arrived, as judged from the typical female call (Crampand Perrins, 1986), or a female with the typical brown morph, werecorded the number of syllables in the presence of the female andthe number in the previous call in the absence of a female. This
allowed us to record the effect of female presence on the numberof syllables. We also recorded the number of males present at thesame time as the focal male was investigated for the number ofsyllables. This allowed us to estimate how the number of syllables
depended on the number of male competitors present at a single
site.
When the number of syllables was recorded, we also noted date,time of day, temperature (measured with a thermometer to thenearest ◦ C), wind (on the Beaufort scale from 0 to 12), cloud cover(estimated in eighths of the sky covered with clouds), and precipitation (either rain or no rain). There were no clear effects ofweather conditions, and these variables were thus excluded from
subsequent analyses. Finally, we recorded whether the cuckoo was
located in agricultural habitats (meadows) or forest. Furthermore,
we recorded whether the soil was sand or black soil. We took greatcare not to include the same male more than once, moving at leasta distance of 500 m before making a subsequent record of the number of syllables in a call. This distance is consistent with distances
between neighboring male cuckoos as recorded in studies based onradio-telemetry (Wyllie, 1981).
2.3. Cuckoo hosts
In Ukraine common cuckoo hosts include the great reed warbler Acrocephalus arundinaceus (89 out of 390 cuckoo eggs) and themarsh warbler Acrocephalus palustris (65 out of 390 eggs), whitewagtail Motacilla alba (35 out of 390 eggs), red-backed shrike Lanius
collurio (31 out of 390 eggs) and robin Erithacus rubecula (20 out of
390 eggs; APM unpublished records).
2.4. Background radiation
Breeding birds generally remain within their territory during thebreeding season (Cramp and Perrins, 1988–1994), and this implies
that all individual birds remain at the site once chosen for reproduction with little heterogeneity in background radiation during
the breeding season. We measured radiation levels in the ﬁeld at
all the survey points, and the radiation level at the actual census
point provides information about the radiation level experienced
by any individuals during breeding due to the sedentary habitsof breeding birds. We measured ˛, ˇ and  radiation at groundlevel at each survey point after having conducted the survey (thusmaking the survey blindly with respect to radiation level) usinga hand-held dosimeter (Model: Inspector, SE International, Inc.,
Summertown, TN, USA). We measured levels several (2–3) times

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at each site one measurement right after another and averaged themeasurements. Our data were validated with correlation against
data from the governmental measurements (Shestopalov, 1996),
estimated as the mid-point of the ranges published, with analyses
showing a high degree of consistency between methods (Møller
and Mousseau, 2007). Radiation levels vary greatly at a local scaledue to heterogeneity in deposition of radioactive material after the
Chernobyl accident (1986). Our measurements at the survey points
ranged from 0.01 to 218.73 ␮Sv/h, which amounts to a difference ofa factor 38,000. Background radiation levels are strongly positively
correlated with internal dose levels for individual birds in Chernobyl (Gaschak et al., 2008). Here, radiation levels are reported as
␮Sv/h as these are the default units provided by most dosimeters(including the ones we use). These units are approximately equivalent to ␮Gy/h, which is the more proper unit when reporting doses
to non-human biota. A recent analysis of doses to Fukushima birds
suggested that ambient radiation measurements are likely to beconservative estimates of individuals doses (Garnier-Laplace et al.,2015).
2.5. Abundance of butterﬂies
We recorded the abundance of butterﬂies during standardized
5-min point counts separated by a distance of 100 m within and justoutside the Chernobyl Exclusion Zone. We have previously reported
the methods and the reductions in abundance of butterﬂies in moreradioactively contaminated sites (Møller and Mousseau, 2009).
2.6. Statistical analyses
We estimated repeatability of the number of syllables in different calls produced by the same male by means of the intraclasscorrelation (Falconer and Mackay, 1996).
Mixed effects models refer to a variety of models, which have asa key feature both ﬁxed and random effects. In this study, Generalized Linear Models were used to study variation in the number ofsyllables in common cuckoo call in relation to environmental variables (habitat and soil type) modeled as ﬁxed effects. Models wereﬁtted by maximum likelihood (Laplace approximations), using the
package ‘lme4’ (Bates et al., 2014) in R, and the minimal models
were chosen using only terms showing a signiﬁcant effect on thepredictor values at a >5% rejection probability. Akaike’s information criterion (AIC) was used for model selection (Burnham andAnderson, 2002). The conﬁdence intervals for the signiﬁcant variables selected in the best model were calculated by the “Wald”
method (Bates et al., 2014). Wald approximates the conﬁdence
intervals (of ﬁxed-effect parameters only) based on the estimatedlocal curvature of the likelihood surface.
In a ﬁrst analysis we studied variation in the number of syllables in the C. canorus call (modeled as a Poisson response variablewith a log link function) in relation to habitat type, type of soil, andpresence of female and male cuckoos. Finally, a GLM procedure wasused to study variation in the number of syllables in the C. canorus
call (modeled as a Poisson response) in relation to radiation levelin sampling sites in Ukraine.
3. Results
3.1. Summary statistics
There was considerable variation in the number of syllables per
call per male cuckoo (Fig. 1). This ranged from 3 to 79, mean 15,
SE = 1.05, N = 129 males. The frequency distribution did not deviatesigniﬁcantly from lognormal (D = 0.066, P = 0.15).

Fig. 1. Frequency distribution of the number of syllables per call in 129 cuckoos.
The red line shows the lognormal distribution. The box plot shows mean, median,quartiles, 5- and 95-percentiles and extreme values. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version ofthis article.)

Table 1
Generalized linear model of the number of syllables per call in relation to habitat,
soil, radiation, time of day, female cuckoo present and number of male cuckoospresent. The syllable variable was treated as count data with a Poisson distribution
and a log link function. The model had the statistics 2 = 878.58, df = 6, P < 0.0001
based on a sample size of 129. Only signiﬁcant variables are shown in the table.
Term

Estimate

SE

2

P

Intercept
Habitat [Forest]
Soil [Sand]
Radiation
Time
Female cuckoo present
No. male cuckoos

2.287−0.1430.197−0.241−0.120
0.400
0.851

0.229
0.036
0.040
0.028
0.019
0.096
0.039

97.85
15.60
26.04
77.65
38.21
15.90
480.37<0.0001<0.0001<0.0001<0.0001<0.0001<0.0001<0.00013.2. Repeatability of number of syllables
Males were signiﬁcantly repeatable in the number of syllables
included in two subsequent calls (F = 4.109, df = 78, 79, r2 = 0.80,
P < 0.001) with the repeatability estimate being 0.61 (SE = 0.10).

3.3. Number of syllables per call and effect of conspeciﬁc females
and males
The number of syllables increased when a female arrived compared to the number of syllables by the same male in the absenceof a female (Table 1; Fig. 2A; paired t-test, t = 2.74, df = 9, P = 0.023).
Males that initially produced many syllables in the absence ofconspeciﬁcs produced disproportionately more syllables in thepresence of a female (F = 23.20, df = 1, 10, r2 = 0.67, P = 0.007, estimate (SE) = 0.77 (0.16)). The number of syllables also increased
linearly with the number of conspeciﬁc males present from 9.3[95% CI = 7.75, 11.16] to 13.6 syllables [11.41, 16.29] (Fig. 2B;
Table 1). Likewise, males that initially produced many syllablesin the absence of conspeciﬁcs still produced more syllables in thepresence of a male (F = 12.60, df = 1, 38, r2 = 0.51, P = 0.0010, estimate(SE) = 0.44 (0.12)).

A.P. Møller et al. / Ecological Indicators 66 (2016) 592–597

595

Fig. 2. The number of syllables in cuckoos from Chernobyl in relation to (A) presence or absence of a female (N = 116 and 13, respectively), (B) number of males present otherthan the focal individual (N = 76, 47 and 6, respectively), (C) soil type (N = 25, 64 and 40, respectively), (D) habitat (N = 96 for forest and 33 for meadows, respectively), (E)time of day (N = 129), and (F) background radiation (␮Sv/h; N = 129). A–D show box plots with medians, quartiles, 5- and 95-percentiles and extreme values, while E and F
show individual observations. The line in (E) is the linear regression line and 95% conﬁdence intervals, while the line in (F) is the regression line Y = 1/X and 95% conﬁdence
intervals.

3.4. Habitat and number of syllables
There were signiﬁcantly more syllables on black soil (21.4 [95%CI = 19.47, 23.62]) than on sand (12.9 syllables [95% CI = 11.97,
13.93]) or on clay (11.2 syllables [95% CI = 9.87, 12.68]) (Fig. 2C;
Table 1). There were more butterﬂies on black soil (2 = 76.23,
df = 2, P < 0.0001, 1.60 [95% CI = 1.25, 1.94]) than on sand (0.47[95% CI = 0.40, 0.53]) and clay (0.21 [95% CI = 0.05, 0.38]). Likewise,
there were 11.2 syllables [95% CI = 9.87, 12.68] in forests, which are

more than 8.6 syllables in meadows [95% CI = 7.27, 10.28] (Fig. 2D;
Table 1). Finally, the number of syllables decreased during the dayfrom a maximum of 19 [95% CI = 15.75, 23.37] at 4 a.m. to a minimum of 6 syllables at 4 p.m. [95% CI = 5.25, 7.80] (Fig. 2E; Table 1).
3.5. Background radiation, habitats and number of syllables
The number of syllables decreased with increasing backgroundradiation level in Chernobyl (Fig. 2F; Table 1). The predicted number

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A.P. Møller et al. / Ecological Indicators 66 (2016) 592–597

of syllables ranged from 16.28 [95% CI = 13.37, 19.84] at a radiationlevel of 0.01 ␮Sv/h (e.g. typical background radiation level) to lessthan half of that at 7.59 syllables [95% CI = 6.44, 8.94] at a radiationlevel of 100 ␮Sv/h according to the statistical model in Table 1.
APM and TAM recorded a total of six individual cuckoos singing
clearly aberrant calls in areas with high levels of radiation:
1. 1 June 2015, Red Forest: cuck-cuoo-cuoo 18 syllables produced
in a single call;
2. 4 June 2015, Chernobyl: cou-cooo-cou 5 syllables;
3. 31 May 2015, Red Forest: cou-cooo emphasis on second part ofsyllable, 8 syllables;
4. 30 May 2013, Red Forest: cou-cooo emphasis on second part ofsyllable, 3 syllables;
5. 28 May 2009, Red Forest: cou-cooo emphasis on second part ofsyllable, 5 syllables; and6. 25 May 2006, Red Forest: cou-cooo emphasis on second part ofsyllable, 10 syllables.
All six cuckoos with aberrant calls were recorded in contaminated areas, which differed signiﬁcantly from random expectation(likelihood ratio = 20.73, P < 0.0001). The mean number of syllables
produced by males with aberrant call (SE) was 8.17 (2.21), N = 6,
differing signiﬁcantly from the overall mean number of syllables of
16 (one-sample t-test, t = −3.09, df = 5, P = 0.027).
4. Discussion
Male cuckoos were consistent in the number of syllables in theircalls. There were fewer syllables and more aberrant syllables inradioactively contaminated areas of Chernobyl compared to control
areas. In addition, the number of syllables differed among habitats
and soil types, showing that at least three components of environmental variation were linked to the production of more syllables.
Cuckoos used their calls in a sexual context because males produced
calls with more syllables especially when a female, but also whenanother male was present. The increase in number of syllables in
the presence compared to the absence of a conspeciﬁc depended on
the initial number of syllables. Males that initially sang many syllables increased the number of syllables in the presence of a female
cuckoo or another male cuckoo. These ﬁndings are consistent with
our hypothesis that the number of syllables is a reliable indicator of environmental condition as reﬂected by the correlations
with habitat, soil type and radioactivity. Likewise, it is consistent
with our hypothesis that the number of syllables is an indicator ofindividual condition as reﬂected by males with many syllables intheir calls being able to disproportionately increase the number ofthe syllables in their calls in the presence of a female or anothermale.
If a signal reliably transmits information on condition or phenotypic quality, we should expect that it is signiﬁcantly repeatable(Searcy and Nowicki, 2005). Here we recorded the number of syllables in two successive calls of a number of male cuckoos andwe showed a signiﬁcant repeatability of 0.61, which is high for abehavioral character (Bell et al., 2009). That was the case despite thefact that the number of syllables produced by any given male alsochanged in response to the number of males and females present
in the immediate neighborhood. Such consistency in the numberof syllables in two subsequent songs implies that inherent qualityof males is reliably reﬂected in calls. Otherwise males that produce
calls with many syllables would not be able to increase the numberof syllables in the presence of conspeciﬁcs.
Syllables of cuckoo calls appear to be associated with sexual
selection. Bird calls have in general evolved in the context of female
choice and male-male competition (Marler and Slabbekoorn, 2004;

Catchpole and Slater, 2008). Our observations showed an effect offemale presence on the number of syllables in calls, suggestingthat the number of syllables may affect mate choice. There wasalso a signiﬁcant relationship between number of syllables and thenumber of competitor males in a given area. Importantly, males
differentially increased the number of syllables in the presence ofa female or a conspeciﬁc male when they initially produced manysyllables in their absence. This ﬁnding is consistent with predictions from the handicap principle (Zahavi, 1975; Johnstone, 1995)
according to which only signallers in prime condition are able todisplay at the highest level. It differs from the alternative hypothesis that motivation accounts for the increase in number of syllablesin the presence of a female or a conspeciﬁc male because thishypothesis would not predict a differential increase in number ofsyllables in males that already sing at a high rate. This suggeststhat both female choice and male-male competition may affect the
number of syllables in cuckoo calls, and that the handicap principle may account for the difference in number of syllables among
males.
If the number of syllables is a reliable indicator of condition, we
should expect that environmental factors affect the expression of
the signal. Here we have shown that ionizing radiation at Chernobyl affects the frequency of individuals with aberrant calls, butalso the number of syllables, which increased from an average of 8syllables in the most contaminated areas to 16 syllables in the least
contaminated areas. Even in the sample of cuckoos with aberrant
call was there a reduction in the number of syllables compared to
expectation for Chernobyl. This implies that different aspects of thecall were affected by ionizing radiation. While ionizing radiation isan uncommon environmental factor, studies of natural radiation
hotspots have shown a diversity of negative phenotypic effects inboth plants and animals including humans (Møller and Mousseau,
2013). We hypothesize that the number of syllables and their structure may depend on mutations and/or on oxidative stress causedby radiation. The effect of environmental conditions on the numberof syllables produced by cuckoos was also supported by the number of syllables differing among habitats and soil types, potentiallymediated by abundance and availability of food. Higher soil quality
increases primary productivity (Begon et al., 2005), which in turnaffects the abundance of herbivores such as butterﬂies (Begon et al.,2005) whose caterpillars constitute the main component of the dietof cuckoos (Cramp and Perrins, 1986). We found evidence consistent with this interpretation because the abundance of butterﬂies
was indeed higher in sites with black soil compared to clay andsand. The association between soil type and abundance of cuckoo
calls may arise from more intense competition for sites with highabundance of food, high abundance of hosts for the brood parasitic cuckoo, or both. Our data do not readily allow discrimination
between these hypotheses.
Previous studies have shown that the presence of cuckoos is areliable indicator of the density of cuckoo hosts and hence of avian
species richness (Morelli et al., 2015; Tryjanowski and Morelli,2015). Given that calls with more syllables would reﬂect superior phenotypic quality of singing males, as shown in the present
study, this suggests that the number of syllables in the calls of
cuckoos is a reliable indicator of condition and environmental
conditions.

Acknowledgments
We gratefully acknowledge logistic support and help in Ukraine
by I. Chizhevsky, G. Milinevski, L. Milinevski and A. Peklo. The
research was conducted with permission from the Ukrainian
authorities. Two anonymous reviewers provided constructive comments.

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