acta ethologica (2020) 23:143–154

https://doi.org/10.1007/s10211-020-00347-6

ORIGINAL PAPER

Two songbird species show subordinate responses to simulated

territorial intrusions of an exotic competitor
Pedro Filipe Pereira 1 & Rui Lourenço 1 & Paulo Gama Mota 2,3

Received: 2 April 2019 / Revised: 1 June 2020 / Accepted: 9 June 2020 / Published online: 23 June 2020
# ISPA, CRL 2020

Abstract
Interspecific competition is rarely assessed between exotic and distantly related native species, although these can compete for
some ecological resources. Here, we assessed the occurrence of interspecific aggression resulting from direct competition
between two European native songbird species (henceforth focal species), the robin Erithacus rubecula and the blackcap
Sylvia atricapilla, which are potential competitors for feeding resources and behaviourally subordinate to the exotic red-billed
leiothrix Leiothrix lutea. In central Portugal, this exotic species lives in sympatry with robins and blackcaps at least since 2007.
We used interactive playbacks to measure the behavioural response of blackcaps and robins towards intrusions by leiothrix and a
submissive, native competitor—great tit Parus major. The singing behaviour of both focal species was affected by leiothrix
playback. Robins exhibited a longer latency to sing, and both species avoided singing near the loudspeaker after leiothrix
playback compared with great tit playback, which generally suggests a subordinate behaviour. Regarding changes in song
parameters during the playbacks, only the peak frequency of blackcaps was affected by the playback. We discuss different
possibilities for the origin of such submissive behaviour in native species.

Keywords Aggressiveness . Competition . Introduced . Leiothrix lutea . Red-billed leiothrix . Song

Introduction in Amarasekare 2003). Often, between-species territoriality

is also observed to mediate conflicts to obtain exclusive access
Interspecific competition is an important factor affecting the to resources (Cody 1978; Losin et al. 2016).
distribution of species and the fitness of individuals (Freed Some successfully established exotic species are dominant
and Cann 2009; Pigot and Tobias 2013). However, the co- over native species and compete aggressively with them,
occurrence of species is not a proof of the absence of compe- which may result in species replacement in natural habitats
tition between them, since overlapping interests will cause (Gurevitch and Padilla 2004; Chapple et al. 2012; reviewed
some sort of conflict (e.g. displacement of inferior in Hudina and Hock 2014). These introductions provide op-
competitors or competition for limiting resources; reviewed portunities for testing how native species react to newly ar-
rived competitors and respond to non-co-evolved aggressive
Responsible editor: Peter McGregor signals, since they often aggressively compete for resources
(Tanner and Adler 2009; Chapple et al. 2012; reviewed in
* Pedro Filipe Pereira Hudina and Hock 2014).
[email protected] Songs are generally used in birds for mate attraction and
territory defence and can signal an agonistic intent (Funghi
1
MED – Mediterranean Institute for Agriculture, Environment and et al. 2015b; reviewed in Searcy and Beecher 2009). Vocal
Development, LabOr – Laboratory of Ornithology, Instituto de interactions between territorial birds can arise within their
Investigação e Formação Avançada, Universidade de Évora, Pólo da own territorial boundaries or during a territorial intrusion
Mitra, Ap. 94, 7006-554 Évora, Portugal
(Naguib 2005). In general, territorial intrusions indicate higher
2
Research Center in Biodiversity and Genetic Resources (CIBIO), arousal of the individual disputing the territory (the intruder)
University of Porto, Campus Agrário de Vairão,
4485-661 Vairão, Portugal
than vocal interactions without crossing territorial boundaries
3
(e.g. Martin et al. 1996; Dabelsteen et al. 1997; Matyjasiak
Department of Life Sciences, University of Coimbra,
3000-456 Coimbra, Portugal
2005; Reif et al. 2015). When the intruder is identified by the
144 acta ethol (2020) 23:143–154

territorial owner as submissive, the owner can show dominant Hawaii and Reunion Island) where it competes with native
behaviour by approaching its intruding opponent, by overlap- species for ecological resources (food and nesting habitat;
ping its songs or by singing immediately after it (Martin et al. Pereira et al. 2017, 2018; Pagani-Núñez et al. 2018; reviewed
1996; Mathevon and Aubin 2001; Briefer et al. 2008; Freeman in Martin-Albarracin et al. 2015). In Europe, the species is
2016). In some cases, singing behaviour is also used to show an established in France, Italy, Spain and Portugal and has dou-
agonistic intent towards a heterospecific competitor (Cody bled its distribution range in the last two decades (Pereira et al.
1978; Martin et al. 1996; Matyjasiak 2005; Reif et al. 2015). 2020). Besides, leiothrix seem to compete with native species
Simulated territorial intrusions using song playbacks are for acoustic space (Farina et al. 2013; Farina and Pieretti
widely experimentally used to measure aggressive responses 2014). Accordingly, leiothrix sing more frequently than most
in territorial bird species (reviewed in Searcy and Beecher European species and its main singing period has a large over-
2009). Some authors have suggested that song overlap is an lap (both daily and seasonally) with some native species (e.g.
aggressive signal between birds as a playback that overlaps robin Erithacus rubecula; Farina et al. 2013). Vocal competi-
the song of a territorial bird (termed overlapping playback) is a tion may even lead to acoustic niche exclusion (e.g. native
way to elicit an aggressive response from the territory owner blackcaps Sylvia atricapilla sing only in the acoustic space
(Dabelsteen et al. 1997; reviewed in Naguib and Mennill left free by exotic leiothrix and do not overlap their songs;
2010). However, the simulation of territorial intrusions using Farina and Pieretti 2014). In other cases, the loss of acoustic
song playbacks of heterospecifics has been mostly applied space by the submissive species can compromise its intraspe-
between species with long-term co-evolution rather than be- cific communication and ultimately results in a reduction of
tween species with a very recent contact as a result of a territory size or mating success (Doutrelant et al. 2000).
human-mediated introduction (Robinson and Terborgh Therefore, it is important to clarify if native species identify
1995; Matyjasiak 2005; Reif et al. 2015; Freeman 2016). a recently introduced species as a dominant competitor and if
Thus, there is a great uncertainty about the response of indi- they adjust their behaviour towards the presence of the intro-
viduals towards non-co-evolved signals of recently arrived duced species regarding ecological or vocal competition. As
competitors, particularly when resources are limited (Bleach focal species, we selected two songbirds—the robin and the
et al. 2015; Tennessen et al. 2016; reviewed in Peiman and blackcap—which are similar to leiothrix regarding their body
Robinson 2010; Grether et al. 2017). size, feeding habits (insectivorous-frugivorous), foraging
The current knowledge on territorial behaviour and ecolo- technique (mostly gleaning) and nesting habitats (open-cup
gy of insectivorous songbirds makes them suitable to study nests in densely vegetated sites; Vall-Llosera et al. 2016;
interspecific competition and aggressiveness because they Pereira et al. 2017; Pagani-Núñez et al. 2018). Robins and
feed on more evenly distributed resources, which are easier blackcaps are suitable models for a study with simulated ter-
to monopolize, than gregarious bird species (Waser and Wiley ritorial intrusions considering they are common European pas-
1979; Funghi et al. 2015a; examples of interspecific competi- serines, with relatively small breeding territories (often <
tion among insectivorous birds: Sylviidae—Cody 1978; 0.5 ha) and fast aggressive response to territorial intrusions
Matyjasiak 2005; Muscicapidae—Reif et al. 2015; Parulidae from conspecifics (Cramp and Perrins 1994; Dabelsteen
and others—Martin et al. 1996; Losin et al. 2016). However, et al. 1997; Matyjasiak 2005). Robins and blackcaps are res-
the existence of territoriality between heterospecifics in bird ident and philopatric species (i.e. use the same territory every
communities invaded by behaviourally dominant exotic bird breeding season) that start breeding in their first year and have
species is not yet well understood because most studies fo- about 2–3 years of life expectancy (Pérez-Tris and Tellería
cused (1) on the perspective of the exotic species as the ag- 2002; PFP unpublished data). In a previous experiment
gressor and (2) on the disputes for specific locations (e.g. tree analysing heterospecific interactions for food, leiothrix initiat-
holes) rather than for the whole territorial space (Lowe et al. ed most interactions and won more frequently against these
2011; Grundy et al. 2014; Hernández-Brito et al. 2014). Here, two native species (Pereira et al. 2018). Besides, population
we wanted to assess the occurrence of interspecific aggression declines or great inter-annual variations in the abundance of
resulting from direct competition for ecological resources (e.g. native passerines have been recorded in regions invaded by
nesting and food resources) from two European native passer- leiothrix (Farina et al. 2013; Farina and Pieretti 2014; Vall-
ines (henceforth focal species) towards a dominant and inva- Llosera et al. 2016). Contrary to most invasive bird species,
sive competitor species using simulated territorial intrusions. leiothrix prefers colonising natural habitats rather than human-
The exotic species considered was the red-billed leiothrix made habitats, which may increase its impact on native spe-
(henceforward leiothrix; Leiothrix lutea; family Timaliidae), cies (Herrando et al. 2010; Vall-Llosera et al. 2016; Pereira
which is a passerine introduced from Asia in several European et al. 2020; reviewed in Martin-Albarracin et al. 2015).
countries (Herrando et al. 2010; Dubois et al. 2016; Pereira This study was designed to determine if individuals of two
et al. 2017; Ramellini et al. 2020). Leiothrix is considered as European native species respond with submissive behaviour
invasive species in four world regions (Europe, Japan, the towards a behaviourally dominant exotic species and if their
acta ethol (2020) 23:143–154 145

responses suggest that they identified the simulated presence delimited the territorial boundaries of a subsample of territo-
of an exotic species as a challenge from a territorial trespasser. rial robins and blackcaps and attributed 32 focal individuals
To measure the singing response of the two native species for testing: 16 male robins and 16 male blackcaps.
towards the exotic species, we simulated intrusions in the
territory of focal individuals using two types of interactive Song recordings
playbacks: (i) a behavioural-dominant species (the leiothrix)
and (ii) a submissive control native species. As control spe- We generated playback stimuli of leiothrix and great tits from
cies, we used the great tit Parus major, a native songbird high-quality recordings without overlapping vocalisations of
considered a submissive competitor (for feeding resources) other individuals, which were collected at least 5 km away
towards the robin and the blackcap without competing for from the study area to reduce the probability of familiarity
nesting sites because it is a tree hole nester (Leach 1981; with the focal individuals. Recordings were collected about
Cramp and Perrins 1994; Vall-Llosera et al. 2016; Francis 5 m distance for all individuals of great tit and leiothrix. A
et al. 2018). We expected both focal species to show different band-pass filter was used to remove the background noise
responses towards the two intruder species with contrasting under 1 kHz and above 10 kHz, and subsequently, the record-
dominance status (i.e. focal individuals can act as dominant or ings were normalised to 90% of the maximum volume in
submissively depending on the intruder species; Miller et al. Avisoft-SASLab Pro (Version 5.2.06, R. Specht, Glienicke,
2017). Considering that song structure similarity (i.e. on fre- Germany). Each stimulus was composed of one repeated song
quency parameters) between singing individuals is an indica- of either a leiothrix or a great tit. We used eight stimuli per
tor of their potential vocal competition (Planqué and intruder species (leiothrix and great tit, 16 stimuli in total; for
Slabbekoorn 2008; Malavasi and Farina 2013; Tobias et al. song examples, see Fig. 1; Table 1).
2014), we also analysed the possibility of vocal competition
by measuring the song structure similarity between focal spe- Simulated territorial intrusions
cies and playbacks and the effect of playbacks on the song
structure of the focal species. Even though vocal competition We simulated intrusions in 16 robin and 16 blackcap terri-
between species has been well documented (Gil and Llusia tories using playbacks of leiothrix and great tit. Intrusion tests
2020), it had not yet been experimentally tested in invaded were performed between 6:00 am and 1:00 pm near the terri-
communities apart from anuran species (Bleach et al. 2015; tory centre of each focal individual. During the test, the ob-
Tennessen et al. 2016). Our results thus bring new insights on server (PFP) remained concealed in the vegetation about 10 m
biotic interference in vocal communication in birds (Gil and away from the speaker and used a remote control to conduct
Llusia 2020). We will discuss the results regarding how native the playback. The observer stayed in the area and conducted a
species can deal with a novel vocal interference with an exotic test successively presenting two playback stimuli, one of each
origin. intruder species. The test included five periods of recording of
the focal individual: (1) spontaneous singing (5 min of singing
including pauses between songs; for song examples, see Fig.
Methods 1; Table 1); (2) playback stimulus of the first intruder species
used to overlap the focal individual’s songs (3 min); (3) a
Study area and territory measurements refractory period (minimum 5 min, and until the focal individ-
ual resumed singing); (4) playback stimulus of the second
The study was performed in central Portugal (40° 3.162′ N, 8° intruder species (i.e. 2nd period); and (5) second refractory
20.540′ W) in a small stream valley bordered by dense and period (i.e. 3rd period). To simulate territorial intrusions for
diverse oak-woodland (Quercus robur). An introduced popu- each intruder species, we used the playback of a song and
lation of leiothrix was discovered in the region in 2007 simultaneously exhibited a plaster hand-painted dummy of
(Matias 2010). In 2015, the population of leiothrix was esti- the intruder species placed in a 1.7-m-high artificial tree
mated at 30 individuals in the study area (28 ha). (15 cm above to the loudspeaker). We used only one dummy
Fieldwork was performed during the breeding season of per intruder species (both male individuals). To reduce possi-
robins and blackcaps, from 6 May to 20 June 2015. All terri- ble effects between consecutive playbacks on the response of
tories of robins and blackcaps were identified within the re- the focal individual, the order of presentation of each intruder
gion occupied by leiothrix using a minimum of nine linear species was randomised. A blindly selected stimulus was
transects. In each territory, we monitored the singing perches played by overlapping the songs of each focal individual dur-
of blackcaps and robins for at least three consecutive days (up ing 3 min from a Sony SRS-A 57 loudspeaker at a peak vol-
to 5 days; three visits per day) and used this information to ume of 80 dB, measured at 1 m to the speaker (a usual
determine the territorial boundaries (adapted from Bibby et al. measure for a great tit song without sexual intent; Ritschard
2000; Reif et al. 2015). As a result of this methodology, we et al. 2012) with a Tenma RS-232 72-860A Sound Level
146 acta ethol (2020) 23:143–154

Fig. 1 Representative spectrograms of songs of the bird species used, Glienicke, Germany) with the following settings: FFT 512; frame size
based on songs used in the playbacks for the red-billed leiothrix and the 75%; Window: Hann; overlap 87.5; sampling frequency 22 kHz;
great tit, and from spontaneous song recordings for the blackcap and the frequency resolution—bandwidth 86 Hz, resolution 43 Hz; temporal
robin generated in Avisoft-SASLab Pro (Version 5.2.06, R. Specht, resolution—1/bandwidth 11.6 ms, resolution 2.9025 ms

Meter (Tenma, Taipei, Taiwan). The average interval between microphone (Sennheiser MKH 70 P48, Wedermark-
playback stimuli presentation was 47.7 min (SD 29.7; range Wennenbostel, Germany) and a portable digital recorder
16.0–129.0 min). The interval between playback stimuli (Marantz Professional PMD661 MKII, Kanagawa,
depended on the time taken by the focal birds to resume sing- Japan). The observer also measured three variables de-
ing and to move enough distance from the artificial tree so that scribing the singing behaviour of focal individuals dur-
the observer could approach to switch the dummy. Focal in- ing each experimental period: (1) minimum distance to
dividuals became silent after the playback presentation in six the loudspeaker (in metres) during the 3 min of play-
intrusion tests; the observer thus extended the recording peri- back; (2) latency to sing (in seconds), as the time until
od until the first song was produced in order to measure the the first song of the focal individual after the end of the
latency to sing after the playback (to a maximum of 7:15 playback; and (3) presence/absence singing within 10 m
minutes:seconds). There was no attack to the dummies by of the speaker (binary variable) during the 5 min fol-
focal individuals in any intrusion test. The guidelines of ex- lowing the playback. Studies measuring the singing be-
periments followed the Directive 2010/63/EU. haviour of robins and blackcaps submitted to simulated
territorial intrusions suggested that quickly approaching
Behavioural responses the loudspeaker and singing close to it is a signal of
dominance over the intruder (Brindley 1991; Hoi-
The singing behaviour of the focal individuals was re- Leitner et al. 1995; Dabelsteen et al. 1997; Matyjasiak
corded all along the test with a directional long shotgun 2004; Darolová et al. 2020).

Table 1 Structure of songs of the focal individuals and the two species playbacks regarding the minimum frequency, maximum frequency and peak
frequency of songs (mean ± standard error)

Minimum frequency (kHz) Maximum frequency (kHz) Maximum peak frequency (kHz) Sample size

Leiothrix playback 1.36 ± 0.48 3.98 ± 1.41 2.79 ± 0.99 8

Great tit playback 2.76 ± 0.98 6.23 ± 2.20 3.99 ± 1.41 8
Spontaneous blackcap song 1.79 ± 0.26 7.82 ± 1.13 3.54 ± 0.51 48
Blackcap song after leiothrix playback 1.84 ± 0.27 7.80 ± 1.16 3.31 ± 0.49 45
Blackcap song after great tit playback 1.84 ± 0.27 7.81 ± 1.16 3.45 ± 0.51 45
Spontaneous robin song 2.56 ± 0.37 8.87 ± 1.28 3.80 ± 0.55 48
Robin song after leiothrix playback 2.61 ± 0.42 9.07 ± 1.45 3.98 ± 0.64 39
Robin song after great tit playback 2.47 ± 0.40 8.64 ± 1.38 4.03 ± 0.65 39
acta ethol (2020) 23:143–154 147

Acoustic interference (two focal species and two intruder species) in the PCA were
used to measure the Euclidean distance between them,
Overlapping of songs may not only signal agonistic or terri- which is considered a suitable measure of song similar-
torial behaviour but can also be a source of signal jamming, ity (Wheatcroft and Price 2013; Xia et al. 2018). The
particularly when individuals compete for acoustic space first component of the PCA describing song similarity
(Brumm 2006; Malavasi and Farina 2013). As competition explained 56.0% of the overall variation and had a
for acoustic space can mask an aggressive response mediating strong and positive correlation with the three frequency
competition for ecological resources (Goodwin and Podos parameters (Table 2).
2013; Tobias et al. 2014), we analysed the possible acoustic We measured the acoustic interference of each intruder
interference of the playback on focal individual songs to ex- species (leiothrix and great tit) on the song of focal species
clude effects of acoustic competition on behavioural response using three high-quality (without overlapping vocalisations)
of focal species. To do so, for each focal individual, we mea- and randomly selected songs per period (spontaneous song,
sured and compared acoustic parameters of three selected song after the playback of leiothrix and song after the play-
songs per period: spontaneous song, song after leiothrix play- back of great tit). We used a generalised estimating equation
back and song after great tit playback. The acoustic parame- model with normal distribution and exchangeable correlation
ters considered were three frequency variables—maximum, structure to measure the acoustic interference of the intruder
minimum and peak (the frequency at the point of maximum species in minimum frequency, maximum frequency and peak
amplitude of the songs in kilohertz). The acoustic parameters frequency of focal species. The individual was used as random
were analysed using Avisoft-SASLab Pro by automatically factor and songs were nested within individuals. All analyses
measuring the parameters on the spectrogram using the were performed using the software R 3.5.2 (R-Core-Team
Pulse Train Analysis function (Fig. 1; Table 1). We visually 2016) with the packages geepack for GEE (Halekoh et al.
controlled all measurements to deal with possible sound 2006), psych for Bartlett’s test of sphericity (Revelle and
distortions. Revelle 2015), rela for KMO (Chajewski 2009) and
FactoMineR for PCA (Husson et al. 2019).
Data analysis

To account for the repeated measures per individuals while Results

testing the effect of the intruder species (leiothrix or great tit)
on the behavioural response of each focal species, we fitted Behavioural responses
three generalised estimating equation (GEE) models with an
exchangeable correlation structure using as response vari- The response of focal blackcaps was different between the
ables: minimum distance (normal distribution after square root playbacks of the two intruder species for the presence singing
transformation), latency to sing (gamma distribution) and within 10 m (Wald χ2 = 7.01, p = 0.008), but we found no
presence singing within 10 m (binomial distribution). GEE differences for other behavioural parameters (Table 3). For
is a powerful tool to analyse behavioural data normally or blackcaps, the probability to come singing within 10 m of
non-normally distributed and including random effects the loudspeaker was lower after the leiothrix playback than
(Pekár and Brabec 2018). Besides the intruder species, we after the great tit playback (Fig. 2). The behavioural response
included the order of the playback (categorical: leiothrix first, of focal robins differed between the playback of the two
great tit first) and the playback time (the time, in minutes,
between the starting hour of the playback and the hour of
the earliest playback among all tests of the study; the start of Table 2 Results of the two first components of principal component
the very first test of the study was attributed zero) to determine analysis of the acoustic parameters of the spontaneous song of focal
individuals and the song playbacks using the minimum frequency,
their possible effect on the behavioural response of the focal maximum frequency and peak frequency. **p < 0.01; ***p < 0.001. For
individuals. The individual was used as a random factor. sample size distribution according to playback type and song structure,
For the analyses of acoustic similarity among species, we see Table 1
performed a principal component analysis (PCA) on the three
Variable Component 1 Component 2
acoustic variables: maximum frequency, minimum frequency
and peak frequency, collected from 96 spontaneous songs of Minimum frequency (correlation) 0.71*** 0.67***
the focal birds (two species) and 16 song stimuli (two intruder Maximum frequency (correlation) 0.74*** − 0.51***
species). We considered reasonable to run a PCA taking into Peak frequency (correlation) 0.79*** − 0.12**
account Bartlett’s test of sphericity: χ2 = 34.88, p < 0.001 and Eigenvalue 1.68 0.72
the KMO = 0.632 for the number of variables and observa- Percentage of explained variance 56.0 24.0
tions (Schumacker 2015). The centroids of the song groups
148 acta ethol (2020) 23:143–154

Table 3 Generalised estimating equations analysing the effect of intruder species, order of the intruder and the playback time in the behavioural
parameters of territorial blackcaps (n = 16) and robins (n = 16). Italic denotes significant values

Focal species Behavioural parameter Explanatory variables Estimate Std. error Wald χ2 p

Blackcap Minimum distance Intercept 3.157 0.156 410.57 < 0.001

Intruder species − 0.089 0.157 0.32 0.571
Order of the intruder 0.317 0.157 4.07 0.044
Playback time 0.001 0.001 0.46 0.500
Latency to sing Intercept 66.177 28.487 5.40 0.020
Intruder species − 8.447 4.528 3.48 0.062
Order of the intruder − 49.845 28.314 3.10 0.078
Playback time − 0.009 0.013 0.41 0.521
Presence singing within 10 m Intercept − 0.234 0.812 0.08 0.773
Intruder species 2.454 0.927 7.01 0.008
Order of the intruder − 1.437 0.926 2.41 0.121
Playback time − 0.002 0.004 0.32 0.570
Robin Minimum distance Intercept 4.186 0.199 440.35 < 0.001
Intruder species − 0.120 0.144 0.70 0.402
Order of the intruder − 0.286 0.132 4.68 0.031
Playback time − 0.001 0.001 3.53 0.060
Latency to sing Intercept 155.618 56.420 7.61 0.006
Intruder species − 3.493 1.637 4.55 0.033
Order of the intruder − 24.977 8.914 7.85 0.005
Playback time − 0.396 0.147 7.26 0.007
Presence singing within 10 m Intercept − 53.873 4.003 181.10 < 0.001
Intruder species 3.063 1.460 4.40 0.036
Order of the intruder 48.366 1.585 930.63 < 0.001
Playback time 0.018 0.010 3.11 0.078

intruder species for the latency to sing and presence singing found that both native species responded differently to the two
within 10 m (Table 3; Fig. 2). Robins showed longer latencies intruder playbacks.
to sing after leiothrix than after great tit (Wald χ2 = 4.55, p =
0.033) and the probability to come singing within 10 m of the Acoustic interference
loudspeaker was lower after the leiothrix playback than after
the great tit playback (Wald χ2 = 4.40, p = 0.036). After ac- The Euclidean distance of the song structure (using the max-
counting for significant playback order effects (Table 3), we imum frequency, minimum frequency and peak frequency)

Fig. 2 Behavioural parameters of focal individuals (blackcaps: n = 16 singing within 10 m (% of individuals). Asterisks denote significant
individuals; robins: n = 16 individuals) measured according to the differences using generalised estimating equations (*p < 0.05;
intruder species: red-billed leiothrix (L) and great tit (T): minimum **p < 0.01)
distance (means ± SE) latency to sing (means ± SE) and presence
acta ethol (2020) 23:143–154 149

was greater (i.e. less similar) between the spontaneous songs (reviewed in Peiman and Robinson 2010; Grether et al.
of focal species and leiothrix playback songs than between the 2017; Ehlman et al. 2019).
spontaneous songs of focal species and the great tit playback
songs (Fig. 3). Regarding changes in song parameters during Competition for acoustic space
the playbacks, only the peak frequency of blackcaps was af-
fected by the playback. Accordingly, blackcaps reduced the Focal birds may suffer from competition for acoustic space as
peak frequencies after the playback of leiothrix when com- a result of the playbacks because the stimuli were played by
pared to their spontaneous songs (Wald χ2 = 4.98, p = 0.026; overlapping their songs, which increases the probability of
Table 4). masking song frequencies and therefore may affect signal
broadcasting and have a detrimental effect on communication
(Brumm 2006; Goodwin and Podos 2013; Malavasi and
Discussion Farina 2013; Farina and Pieretti 2014). If focal birds were
affected by competition for acoustic space by leiothrix more
Our study of the behavioural response to territorial intrusions than by the great tit (the control playback), we would expect
suggests that blackcaps and robins are affected by leiothrix. focal birds (1) to show greater similarity on song structure
Robins exhibited a longer latency to sing and both species (measured using Euclidean distances) with leiothrix than with
avoided singing near the loudspeaker after leiothrix playback great tit (Naugler and Ratcliffe 1994; Planqué and
compared with after great tit playback. The song structure, in Slabbekoorn 2008), (2) to show greater variation in the song
particular the peak frequency, of blackcaps was affected structure after leiothrix playback than after the control play-
by the leiothrix playback. These results suggest a sub- back (Goodwin and Podos 2013; Verzijden et al. 2010), (3) to
missive response of focal individuals towards leiothrix, stay further away from the loudspeaker during the playback of
which can be due to (1) competition for acoustic space, leiothrix songs than during control songs (i.e. the minimum
or (2) identification of a dominant competitor. The two distance during the playback should be longer for the
intruder species differ by more than one criteria (domi- leiothrix); and/or (4) to start singing right after the end of
nant competitor versus submissive competitor and exotic leiothrix playback, which would suggest greater acoustic
opponent versus native opponent) which can be regarded as a competition with leiothrix than with the great tit (i.e. the
limitation of our experimental design. Therefore, we discuss latency to sing after the playback should be shorter for
our results considering two other hypotheses potentially leiothrix; Naguib 2005; Goodwin and Podos 2013;
explaining our results: (3) mistaken identification and (4) McLaughlin and Kunc 2013). The greater song similarity be-
neophobia which are likely to occur between novel opponents, tween leiothrix and blackcaps than leiothrix and robins sug-
such as interactions between exotic and native species gests greater potential acoustic competition with blackcaps.

Fig. 3 Euclidean distances

between the centroids (four large
dots) of spontaneous songs of the
focal individuals (blackcaps
n = 48 songs; robins n = 48 songs)
and the two playbacks (leiothrix
n = 8 songs; great tit n = 8 songs)
using the minimum frequency,
maximum frequency and peak
frequency
150 acta ethol (2020) 23:143–154

Table 4 Generalised estimating equations analysing the effect of songs = 138; robin songs = 123) because focal individuals became silent
intruder species in the acoustic parameters of territorial blackcaps (n = after the playback presentation in six intrusion tests. For sample size
16) and robins (n = 16) using a 3-level condition (spontaneous song, song distribution according to playback type and song structure, see Table 1.
after leiothrix playback and song after great tit playback). We used three Italic denotes significant values
songs per condition. The sample size differed between species (blackcap

Focal species Behavioural Explanatory Estimate Std. error Wald χ2 p

parameter variables

Blackcap Minimum frequency Intercept 1.788 0.040 2072.24 < 0.001

Leiothrix 0.050 0.056 0.80 0.371
Great tit 0.057 0.051 1.24 0.266
Maximum frequency Intercept 7.808 0.224 1220 < 0.001
Leiothrix − 0.004 0.301 0 0.99
Great tit − 0.0003 0.318 0 1.00
Peak frequency Intercept 3.571 0.096 1393.70 < 0.001
Leiothrix − 0.264 0.118 4.98 0.026
Great tit − 0.120 0.125 0.92 0.338
Robin Minimum frequency Intercept 2.536 0.067 1433.30 < 0.001
Leiothrix 0.077 0.098 0.63 0.43
Great tit − 0.066 0.096 0.48 0.49
Maximum frequency Intercept 8.884 0.083 11,483.5 < 0.001
Leiothrix 0.187 0.110 2.9 0.088
Great tit − 0.249 0.172 2.1 0.147
Peak frequency Intercept 3.822 0.062 3833.23 < 0.001
Leiothrix 0.157 0.099 2.52 0.11
Great tit 0.211 0.112 3.53 0.06

Blackcaps sang more frequently away from the loudspeaker it is essential that individuals are familiar with it, which de-
and decreased their peak frequencies after leiothrix playbacks pends on some demographic or ecological attributes such as
which suggests that they were affected by acoustic competi- high abundances, habitat similarities and same temporal activ-
tion with leiothrix more than by acoustic competition with the ity pattern (e.g. Ord et al. 2011; reviewed in Grether et al.
control species. On the contrary, robins and leiothrix do not 2009). Accordingly, focal blackcaps and focal robins should
appear to compete for acoustic space. Even if robins also sang be equally familiar to both intruder species as they share the
further away from the loudspeaker after leiothrix playback same demographic and ecological attributes in the study area.
compared with great tit playback, the simulation of an intru- During encounters (e.g. simultaneous foraging in the same
sion by leiothrix did not affect robin’s song structure and place), individuals can assess the fighting ability of the oppo-
decreased rather than increased robin’s propensity to overlap nents even without engaging in aggressive contests (e.g.
competitor’s songs (as measured by the longer latency to sing evaluating the weaponry by sight; Számadó 2008; reviewed
after the playback). in Arnott and Elwood 2008). The dominance of the leiothrix
can be also inferred by other passerine species through its
Identification of a dominant competitor relatively larger body mass (about 24 g for leiothrix and about
17–18 g for the other three species), which suggests a greater
Another possible explanation for our results is that focal indi- fighting ability than blackcaps, robins and great tits (Cramp
viduals responded differently towards the leiothrix than to- and Perrins 1994; Pereira et al. 2017, 2018). There are some
wards the submissive control species (the great tit) because evidences of a behavioural submission from blackcaps and
they identified leiothrix playback as belonging to a dominant robins towards leiothrix (Farina et al. 2013; Farina and
species (Robinson and Terborgh 1995; Martin et al. 1996; Pieretti 2014; Vall-Llosera et al. 2016; Pereira et al. 2018).
Freeman 2016; reviewed in Grether et al. 2009; Peiman and Moreover, the identification of the leiothrix as a dominant
Robinson 2010). Also, when submitted to leiothrix playbacks, species by blackcaps and robins was observed in an experi-
blackcaps sing only in the space left free by leiothrix indicat- mental study with food supply (Pereira et al. 2018). On the
ing they behave submissively towards the invader (Farina contrary, regardless of identical body masses, the great tits
et al. 2013; Farina and Pieretti 2014). To identify an opponent, have been shown to act submissively against blackcaps and
acta ethol (2020) 23:143–154 151

robins in foraging contexts (Leach 1981; Francis et al. 2018). in response to this novel disturbance (Ehlman et al. 2019),
Longer latencies to sing and avoidance of loudspeaker prox- regardless of the dominance or competitive relationship be-
imity after heterospecific songs are submissive signals wide- tween these species. The absence of familiarity between indi-
spread among passerine birds (Reif et al. 2015; Freeman 2016; viduals can result in avoidance (i.e. neophobia) as have been
Hick et al. 2016; Darolová et al. 2020). Thus, the observation noticed between some native species facing exotic competi-
of these behaviours in our experiments suggests that leiothrix tors (McEvoy et al. 2008; Peck et al. 2014). To fully analyse
playbacks elicit an avoidance response in robins (and possibly the hypothesis of neophobia in our study, it would have been
also in blackcaps) caused by the behavioural dominance of necessary to have four playback treatments: 1 exotic dominant
leiothrix. competitor, 1 native dominant competitor, 1 exotic submissive
competitor and 1 native submissive competitor. Nevertheless,
Mistaken identification it is very likely that all focal individuals in our study (mini-
mum age: a year old) have already encountered at least a
When interacting individuals belonging to different species leiothrix along their life; therefore, the hypothesis of
share some morphological or vocal characteristics, the occur- neophobia can be considered rather unlikely.
rence of misidentification of an opponent as a conspecific op-
ponent may arise (‘mistaken identity hypothesis’; Murray
1971; Robinson and Terborgh 1995; reviewed in Peiman and Conclusions
Robinson 2010). In our case, it is possible that focal individuals
(particularly focal blackcaps) may have misidentified leiothrix To the best of our knowledge, this is the first study focusing
playback as belonging to a conspecific. This is a likely possi- on the impact of an invasive bird species on signalling pro-
bility because the structure of leiothrix song is more similar to cesses of native species. The most relevant result of our study
the blackcap song than to other European species, although was the subordinate response of both blackcaps and robins
differing from the blackcap song through a lower peak frequen- towards an exotic species, regardless of resulting from recog-
cy and lower frequency range (Table 1; Figs. 1 and 3; Martens nition of a dominant species or from a mistaken identification.
and Eck 1995; Matias 2002; Herrando et al. 2010; Cerato and This is supported by the fact that the leiothrix is a very vocal
Fracasso 2014; Ramellini 2017). Considering that blackcaps species, its songs have a great signal broadcast regardless the
identify songs varying greatly in frequency parameters as con- environment and its daily and seasonally singing activity has a
specific songs (Mathevon and Aubin 2001), but also that a great temporal overlap with some European native species
decrease in frequency parameters is an aggressive signal (Farina et al. 2013; Sebastián-González et al. 2018). Also,
expressed in their song (Leedale et al. 2015), it is possible that our results indicate possible competition for acoustic space
blackcaps misidentified leiothrix playback as a conspecific be- between blackcaps and leiothrix. Further experiments are
cause they reduced their peak frequencies after leiothrix. needed to test if individuals from native species respond to a
Moreover, considering the overlapping playback (as performed leiothrix according to its behavioural dominance or because
in this study) to be a more aggressive signal than an alternating they are responding to a novel disturbance. A way forward is
playback (Dabelsteen et al. 1997; reviewed in Naguib and to perform similar approaches to ours in study areas with and
Mennill 2010), this may have contributed to the submissive without the presence of leiothrix or with different times of
response of focal blackcaps towards leiothrix. However, a con- colonisation by the exotic species. These studies may help in
firmation of the ‘mistaken identity hypothesis’ requires to test evaluating the effect of coexistence time on the behavioural
the song similarity between species using some song parame- response between native and exotic competitor species.
ters which were not analysed in this study, such as the syllable Considering that submissive singing behaviour is costly (e.g.
type and the interval among syllables (Tchernichovski et al. reduction of the singing period and of chances of mate
2000; Qvarnström et al. 2006). attraction and territorial defence against conspecifics;
reviewed in Grether et al. 2017; Hau et al. 2017), it would
Neophobia be also relevant to analyse if the presence of leiothrix has a
negative effect on the fitness of native species.
At the species level, a long-term co-evolution among
heterospecific competitors with different social statuses may Acknowledgements We are grateful for the comments and suggestions
of the associate editor Mylene M. Mariette and two anonymous reviewers
force the submissive species to change its behaviour or ecol-
who contributed to improve a previous version of the manuscript. We
ogy (character displacement, when living in sympatry with a thank the LabOr (University of Évora) and CIBIO for logistical support.
dominant competitor) or, ultimately, may lead to its competi-
tive exclusion (reviewed in Grether et al. 2017). At the indi- Funding information PFP was supported by a doctoral grant (SFRH/BD/
vidual level, considering the exotic condition of leiothrix in 87340/2012) and RL by a post-doctoral grant (SFRH/BPD/78241/2011)
from Fundação para a Ciência e a Tecnologia (Portugal POPH/FSE).
our study, focal individuals can show a submissive behaviour
152 acta ethol (2020) 23:143–154

Compliance with ethical standards Freed LA, Cann RL (2009) Negative effects of an introduced bird species
on growth and survival in a native bird community. Curr Biol 19:
1736–1740
Conflict of interest The authors declare that they have no conflict of
interest. Freeman BG (2016) Strong asymmetric interspecific aggression between
two sympatric new Guinean robins. Ibis 158:75–81
Funghi C, Leitão AV, Ferreira AC, Mota PG, Cardoso GC (2015a) Social
Ethics statement All applicable international, national and/or institu-
dominance in a gregarious bird is related to body size but not to
tional guidelines for the care and use of animals were followed.
standard personality assays. Ethology 121:84–93
Funghi C, Cardoso GC, Mota PG (2015b) Increased syllable rate during
aggressive singing in a bird with complex and fast song. J Avian
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