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Crying wolf to a predator: deceptive vocal
mimicry by a bird protecting young
Branislav Igic1,†, Jessica McLachlan1,2, Inkeri Lehtinen1,3
and Robert D. Magrath1
Research
Cite this article: Igic B, McLachlan J,
Lehtinen I, Magrath RD. 2015 Crying wolf to a
predator: deceptive vocal mimicry by a bird
protecting young. Proc. R. Soc. B 282:
20150798.
http://dx.doi.org/10.1098/rspb.2015.0798
Received: 8 April 2015
Accepted: 11 May 2015
Subject Areas:
behaviour, ecology
Keywords:
alarm call, anti-predator, deception,
interspecific eavesdropping, mimicry,
nest defence
Author for correspondence:
Branislav Igic
e-mail: [email protected]
†
Present address: Department of Biology,
University of Akron, Akron, OH 44325 – 3908,
USA.
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2015.0798 or
via http://rspb.royalsocietypublishing.org.
1
Research School of Biology, The Australian National University, Canberra, Australian Capital Territory, Australia
Department of Zoology, University of Cambridge, Cambridge, UK
3
Department of Environmental Sciences, University of Helsinki, Helsinki, Finland
2
Animals often mimic dangerous or toxic species to deter predators; however,
mimicry of such species may not always be possible and mimicry of benign
species seems unlikely to confer anti-predator benefits. We reveal a system in
which a bird mimics the alarm calls of harmless species to fool a predator
40 times its size and protect its offspring against attack. Our experiments
revealed that brown thornbills (Acanthiza pusilla) mimic a chorus of other
species’ aerial alarm calls, a cue of an Accipiter hawk in flight, when predators attack their nest. The absence of any flying predators in this context
implies that these alarms convey deceptive information about the type of
danger present. Experiments on the primary nest predators of thornbills,
pied currawongs (Strepera graculina), revealed that the predators treat these
alarms as if they themselves are threatened by flying hawks, either by scanning the sky for danger or fleeing, confirming a deceptive function. In turn,
these distractions delay attack and provide thornbill nestlings with an
opportunity to escape. This sophisticated defence strategy exploits the complex web of interactions among multiple species across several trophic levels,
and in particular exploits a predator’s ability to eavesdrop on and respond
appropriately to heterospecific alarm calls. Our findings demonstrate that
prey can fool predators by deceptively mimicking alarm calls of harmless
species, suggesting that defensive mimicry could be more widespread
because of indirect effects on predators within a web of eavesdropping.
1. Introduction
Prey animals often use dishonest signals to fool predators and escape predation.
For example, prey species can make themselves appear larger or displeasing,
and thus deter predators from attacking [1,2]. Mimicry is another classic example
of a dishonest signal and is often used by otherwise undefended organisms to
deceive predators into misidentifying them as toxic or dangerous species (defensive mimicry [3]). This is generally accomplished by mimicking attributes of
dangerous models, including predators themselves, or the aposematic coloration
or warning sounds of noxious prey (Batesian mimicry [1,4–6]). However,
mimicking dangerous species is not always possible, and it is unknown whether
mimicking harmless species can provide protection against predators.
Although the protective benefits of traditional examples of mimicry are well
known, such as for Batesian and Müllerian mimicry [7,8], it is still unclear if
avian vocal mimicry has an anti-predator function [9,10]. Mimicry of other
species’ vocalizations or sounds is widespread among songbirds, but the function
of these mimetic vocalizations is known for only a handful of species (reviews:
[9,10]). In response to predators, birds often mimic sounds that are associated
with danger, such as calls of predators or alarm and aggression calls of heterospecifics, suggesting that vocal mimicry confers anti-predator protection by
similar mechanisms as Batesian mimicry [11–14]. Indeed, mimicry of rattlesnake
(Crotalus viridis) rattling sounds by burrowing owls (Athene cunicularia) has been
shown to deter heterospecific competitors from entering owl burrows and thereby
potentially evicting owls [4]. Yet surprisingly, how predators respond to mimetic
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
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(a)
brown goshawk
(top predator)
(b)
16
2
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thornbill alarm
8
honeyeater alarm
8
Proc. R. Soc. B 282: 20150798
frequency (kHz)
pied currawong
(nest predator)
0
16
0
16
mimicry of honeyeater alarm
brown thornbill
(mimic)
New Holland honeyeater
(mimicked species)
8
0
0
0.3
time (s)
0.6
Figure 1. Predator –prey relationships between species, and aerial alarm vocalisations used in experiments. (a) From top to bottom: brown goshawk (top predator),
pied currawong (nest predator), brown thornbill (mimic), New Holland honeyeater (harmless species mimicked); arrows indicate direction of predator– prey relationship. (b) Spectrograms of brown thornbill non-mimetic aerial alarms, New Holland honeyeater aerial alarms and corresponding mimicry by brown thornbills. Photo
credits: brown goshawk, Geoffrey Dabb; rest, Steve Igic. (Online version in colour.)
vocalizations of prey has never been tested. As a result, avian
vocal mimicry is often placed outside the evolutionary framework of traditional mimicry systems (for discussions, see [10,15]).
Alarm calls can be used to deceive competitors, and such
deception can entail non-mimetic or mimetic calls [16–18].
Several bird species produce alarm calls in the absence
of danger to distract competitors and steal their food
(e.g. Dicrurus adsimilis [18]), or use deceptive alarms as a
mate-guarding strategy (e.g. Hirundo rustica [19]). This deception is possible between species because individuals often
eavesdrop on and respond to alarm calls of other species
[20]. There are two main types of avian alarm calls: (i) aerial
alarm calls are produced to predators in flight and provoke listeners to scan the sky or fly into cover, and (ii) mobbing alarm
calls are produced to terrestrial predators or stationary avian predators, and provoke listeners to inspect and harass the predator
[21]. Aerial alarm calls are particularly effective signals for startling others because predators in flight are extremely dangerous
and require listeners to respond immediately [21]. However, just
like the story of the boy who cried wolf, the effectiveness of
deception can decline when deceptive alarms are used too frequently [17,22,23]. Callers can potentially avoid resistance to
deception by mimicking the alarm calls of other species, thereby
reducing the frequency of any one type of deceptive call [17].
Although the use of non-mimetic and mimetic alarms to deceive
competitors is well documented, it is unclear whether alarms of
any type are used to deceive predators.
For most bird species studied, human disturbance or predator attacks on a nest provoke parents to produce mobbing
alarm calls, which is appropriate when predators are not in
flight [21]. However, brown thornbills (Acanthiza pusilla;
figure 1a) mimic a chorus of other species’ aerial alarm calls
when humans disturb their nests [14]. As no flying predator
is present, the production of aerial alarm calls by thornbills
during nest defence conveys inaccurate information about
danger and may serve to deceive predators into responding
as if they themselves are in immediate danger from above
[14,24]. Mimicking a chorus of aerial alarm calls may also simulate multiple callers, a reliable indication of immediate danger
[20,25–27], which may increase the effectiveness of deception.
Here, we experimentally tested the anti-predator function
of mimetic aerial alarm calls used by brown thornbills during
nest defence. We examined the interactions between thornbills
and their primary nest predators, pied currawongs (Strepera
graculina; figure 1a), and tested the hypotheses that (i) thornbills use aerial alarm calls to deceive currawongs that attack
their nest, and that (ii) mimicking a chorus of alarm calls is
better at deceiving currawongs than using a single, nonmimetic type of alarm call. Currawongs are susceptible to
being deceived by aerial alarm calls because they themselves
are prey to Accipiter hawks, such as A. fasciatus (figure 1a;
[28]), which are dangerous top predators that provoke aerial
alarm calls from thornbills and other sympatric species.
2. Material and methods
(a) Study site, species and experimental overview
We studied free-living colour-banded thornbills and unbanded pied
currawongs in and around the Australian National Botanic Gardens,
Canberra, Australia (358160 S, 149860 E). Both species are highly territorial, pair-breeding passerines common throughout southeastern
Australia [29,30]. Brown thornbills are 7 g and build dome-shaped
nests typically 0.5–1 m above the ground and in dense vegetation
[29]. Currawongs are 280 g specialized nest predators that can capture
up to 2 kg of young birds to raise a single brood to maturity [31]. An
estimated 52% of brown thornbill nests with nestlings suffer mortality
at our study site, with 61–83% of these losses attributed to nest
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To test when thornbills use mimetic aerial alarms, we simulated
three levels of threat to 8 – 10-day-old nestlings of breeding thornbill pairs in 2011, approximately 6 days before normal fledging
age. We presented 10 thornbill pairs with taxidermic mounts
1 m in front of their nests in combination with broadcasting
sounds to simulate three levels of threat: (i) no threat control—a
crimson rosella (Platycercus elegans, a harmless sympatric parrot)
near the nest in combination with rosella contact calls, (ii) potential
threat from a searching nest predator—a pied currawong near the
nest in combination with rosella contact calls, and (iii) immediate
threat from a predator attacking the nest—a pied currawong
near the nest in combination with nestling distress calls, which
are produced by nestlings only when disturbed (electronic supplementary material, figure S1). All three treatments were
presented to a pair in random order during a single day. Additional
details of experimental protocol are provided in the electronic supplementary material. To test the specificity of responses in relation
to nestling distress calls, each sound was broadcast only once for 4 s
at the start of a 5 min period when the model was presented.
Sounds were broadcast at the average amplitude of nesting distress
calls (mean ¼ 49.2 dBA from 4 m; s.e.m. ¼ 0.63; n ¼ 10). We
recorded vocalizations produced by parents following protocols
described in Igic & Magrath [14]. For ethical reasons, we conducted
experiments before nestlings were old enough to prematurely
fledge as that may reduce their survival.
We examined production of non-mimetic and mimetic alarm
calls by parents: (i) over the full 5 min threat treatment, and
(ii) specifically during the 4 s period that nestling distress calls
were broadcast, simulating a period of nest attack. We inspected
spectrograms using RAVEN PRO v. 1.4 [34] and identified the calls
produced by parents using protocols described in Igic & Magrath
[14]. We categorized parental calls into five types based on their
use by thornbills and heterospecifics outside the context of nest
defence: non-alarm, non-mimetic mobbing alarm, non-mimetic
aerial alarm, mimetic mobbing alarm and mimetic aerial alarm
[14]. Summaries of the thornbill’s mimetic repertoire are presented in Igic & Magrath [14,24]. Thornbills rarely mimic
predator calls [14], and never did so in this study. Both parents
were present during our experiments and we considered their
combined call production in analyses. Mimicry of aerial alarms
when a currawong is nearby but young are undisturbed would
suggest a function in hindering predators from finding the
nest, whereas mimicry during the simulated attack would
suggest a function in helping young escape.
(c) Currawong response to thornbill alarms at simulated
nests
Next, we tested how currawongs themselves respond to thornbill
non-mimetic and mimetic aerial alarm calls. We broadcast three
sets of 4 s thornbill vocalizations to 18 currawongs during their
breeding season in 2011: (i) non-mimetic aerial alarms alone, (ii) a
combination of non-mimetic and mimetic aerial alarms, and
(d) Currawong response to thornbill and real
honeyeater alarms
We conducted a follow-up experiment in 2013 to examine how currawongs respond to New Holland honeyeater aerial alarms and test
whether these alarms are more salient to them than thornbill alarms.
Currawongs might respond more strongly to a mixture of nonmimetic and mimetic alarms than non-mimetic alarms alone
because (i) the mimetic alarm itself is more salient or (ii) the mixture
of different species’ alarms is more salient than alarms of a single
species. We therefore broadcast four types of calls alone over 0.8 s
to currawongs feeding in the open: (i) thornbill song as a control,
(ii) thornbill non-mimetic aerial alarms, (iii) thornbill mimetic honeyeater aerial alarms, and (iv) the honeyeater’s own aerial alarms
(figure 1b). We used the same currawong population as in the previous experiment, but only 10 pairs produced nests during 2013
and could be used for this experiment.
We used a modified protocol compared with the previous
experiment. We placed food on the ground, rather than in a
feeder, to examine the salience of alarms as opposed to their effectiveness in nest defence. Recordings were broadcast using the
same equipment and methods, but the equipment was mounted
around the waist of an observer standing 10 m away from the
focal bird. We again video recorded currawong responses and
3
Proc. R. Soc. B 282: 20150798
(b) Thornbill response to nest threat
(iii) thornbill song as a control. We used a mixture of non-mimetic
and mimetic alarms, rather than mimetic alarms alone, because
thornbills generally use mimetic alarms in combination with nonmimetic alarms [14]. For mimetic alarms, we used mimicry of
New Holland honeyeater (Phylidonyris novaehollandiae) aerial
alarm calls, the call most frequently mimicked during nest defence
[14]. We predicted that the aerial alarms would distract currawongs
and that mimicry would prolong this distraction. Under natural circumstances, a delay would allow older thornbill nestlings to
scramble out of the nest and hide in surrounding vegetation [29].
We trained currawongs to feed from custom-made feeders that
simulated a thornbill nest environment (electronic supplementary
material, figure S2), where we broadcast the recordings of thornbill
vocalizations. Full details of training protocol and creation of
playbacks are provided in the electronic supplementary material.
Once currawongs were habituated to feeders and our experimental
equipment, we broadcast each recording on a separate date, in
random order, and in the absence of species aggressive towards
currawongs or any aerial alarm calls nearby in the previous
10 min. Upon setting up the feeder and equipment, we allowed
currawongs to make two visits to the feeder before broadcasting
a recording the moment a currawong was about to pick up food
on its next visit. All recordings were broadcast from a Response
Dome Tweeter speaker mounted on a tripod 0.7 m from the
ground and 5 m from the feeder. We played sounds from an
Edirol R-09HR solid-state digital player and custom-built amplifier
at an amplitude of 60 dBA at 5 m (average amplitude of thornbill
aerial alarms recorded during nestling banding [14]), and we
video recorded currawong behaviour.
We examined how currawongs responded to playbacks by analysing video recordings using MICROSOFT WINDOWS MOVIE MAKER v.
2.6 (Microsoft Corporation). We classified the immediate behaviour
of currawongs following sounds into three categories that reflected
the intensity of their alarm response: flight from the feeder’s
location, aerial scanning (defined as looking up for more than
1 s), or other response. Currawong behaviour was classified into
these categories by a scorer blind to the playback treatment: the
video recordings were in random order, the sound was muted
and the timing of playbacks was marked visually. The intensity
of an individual’s alarm response can also be measured as the
delay until their behaviour returns to normal (e.g. [35,36]), so we
also measured how long currawongs delayed collecting food
after playbacks, again using blind scoring (to the nearest 0.1 s).
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predation by avian predators, primarily pied currawongs [32]. There
are no data on the rate of predation by hawks for either species; however, the annual rate of survival for brown thornbills and pied
currawongs is, respectively, 63% and 82% [32,33].
To test our hypotheses, we first tested experimentally whether
thornbills mimic aerial alarm calls in response to currawongs on
the ground during nest defence, and if so whether these are likely
to function in preventing attack or helping young escape when
attacked. We then tested whether currawongs are deceived by thornbill alarm calls and mimicry at simulated thornbill nests. Finally, we
examined the response by currawongs to thornbill, heterospecific,
and mimetic alarms to test their salience when broadcast alone.
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(a)
(b)
20
(c)
25
20
10
5
0
15
10
150
100
50
5
0
0
0
30 60 90 120 150 180 210 240 270 300
time (s)
no
threat
potential
threat
immediate
threat
Figure 2. Alarm calling by thornbills during nest threats. (a) Alarm calls (fitted means + s.e.m.) produced by thornbills (n ¼ 10) specifically during the 4 s in which
nestling distress calls were broadcast: simulated attack on the nest. (b) Alarm calls (mean + s.e.m.) produced by thornbills (n ¼ 10) at every 15 s interval following a
simulated attack on the nest by a predator. Arrow indicates the period when nestling distress calls were broadcast (simulated attack on the nest). (c) Calls (mean +
s.e.m.) produced by thornbills (n ¼ 10) over 5 min in response to different levels of threat: no threat; potential threat—a predator near the nest; and immediate
threat—following a simulated attack on the nest by a predator. Analyses are shown in the electronic supplementary material, tables S1–S3. (Online version in colour.)
used blind scoring to classify the initial response of currawongs
to playbacks and the amount of time they spent aerial scanning
following alarm calls (to the 0.1 s).
(e) Statistical analyses
We used statistical models to compare the number and types of
alarm calls produced by parents: (i) in response to the three levels
of threat over the full 5 min, and (ii) specifically during 4 s of
nestling distress calls. Analyses compared: (i) the long-term
responses of parents to degrees of nest threat, and (ii) the specific
response of parents during nest attack. For the long-term response
(i), we constructed a general linear model with the number of
alarm calls produced by parents over 5 min as a response; pair
ID, treatment order, threat type, alarm call type, and the interaction between threat type and alarm call type as covariates. To
improve fit we transformed the response (log10 þ 1). The interaction between alarm call type and threat type was significant
(electronic supplementary material, table S1) indicating that the
four types of alarm calls were used differently across threat treatments. Therefore, we constructed separate linear models to
compare production of alarm calls during potential and immediate threats. We used the log number of alarm calls as a response;
pair ID and alarm call type as covariates (electronic supplementary material, table S2). For the short-term response to nest
attack (ii), we used a zero-inflated negative binomial (ZINB)
model to test if mimetic aerial alarm calls were used more frequently than other alarms during the 4 s of nestling distress calls
(electronic supplementary material, table S3). Parents did not produce any calls during 4 s of rosella calls, and therefore this
treatment could not be included in the analysis. We constructed
this model with the number of alarm calls produced during the
4 s as a response; alarm call type and pair ID as fixed effects.
A ZINB model fitted our data better than a negative binomial
model (Vuong closeness test: V ¼ 23.82, p , 0.001; [37]).
We compared currawong responses to playbacks using
McNemar’s tests and linear mixed models. We used McNemar’s
tests to compare categorical responses of currawongs to playbacks
(fleeing, aerial scanning or other non-aerial-specific response).
We constructed linear mixed models to compare the latency for
currawongs to resume feeding after playbacks (electronic supplementary material, table S4) or time spent scanning (electronic
supplementary material, table S5). Currawongs never scanned
the sky following song in the second experiment (electronic supplementary material, figure S3), so this control treatment was
not included in subsequent analysis. We used the time currawongs
delayed feeding or spent scanning following a playback as
responses, recording type and playback order as fixed effects,
and currawong identities as random effects. To alleviate problems
with unequal variances, we square-root transformed the latency
for currawongs to resume feeding.
All statistical analyses were conducted in R [38]. We constructed linear mixed models using identity link functions,
REML and the lme() function of the nlme package [39]. Our
ZINB model was constructed using the zeroinfl() function and
we conducted Vuong closeness tests using the vuong() function,
both from the pscl package [40]. For each model, we visually
checked violations of normality and equality of variance using
q–q normal plots and residuals plots. We used ANOVA and likelihood ratio tests to identify significant effects, and conducted
pairwise post hoc tests and Tukey contrasts using the glht() function of the multcomp package [41]. McNemar’s tests were
conducted using the mcnemar.test() function [38].
3. Results
In support of a function in helping young escape when
attacked, thornbills mimicked heterospecific aerial alarm calls
specifically during simulated nest attack, and not when a predator model was merely nearby. Mimetic aerial alarms were
used despite the absence of a flying predator and were the
most common type of call used by parents during the playback
of nestling distress calls (ZINB effect: x26 ¼ 20:85, p , 0.01;
all post hoc comparisons, p , 0.05; figure 2a; electronic
supplementary material, table S3). Mimicry of aerial alarms
coincided specifically with the 4 s that nestling distress
calls were broadcast (figure 2b), beginning on average 1.9 s
(+1.1 s.e.m.) after the onset of nestling distress calls and continuing for an average 5.9 s (+3.2 s.e.m.). During this time,
parents mimicked between one and four different species’
aerial alarms (average 1.9 + 0.4 s.e.m.). After the simulated
attack had finished or when a currawong was merely present
nearby, parents produced non-mimetic and mimetic mobbing
alarms, such that over the full 5 min mimetic aerial alarm
calls were used less often than non-mimetic (potential threat:
t27 ¼ 10.28, p , 0.001; immediate threat: t27 ¼ 4.44, p , 0.001)
and mimetic ( potential threat: t27 ¼ 7.43, p , 0.001; immediate
threat: t27 ¼ 2.82, p ¼ 0.04) mobbing alarms (figure 2b,c;
electronic supplementary material, tables S1 and S2).
Proc. R. Soc. B 282: 20150798
non-mimetic mimetic non-mimetic mimetic
mobbing mobbing
aerial
aerial
200
no. vocalizations
no. alarm calls
no. alarm calls
15
4
non-alarm
non-mimetic mobbing
mimetic mobbing
non-mimetic aerial
mimetic aerial
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non-mimetic mobbing
mimetic mobbing
non-mimetic aerial
mimetic aerial
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(a)
(b)
20
15
10
5
time spent scanning (s)
latency to resume feeding (s)
aerial scan
flight
other response
8
aerial scan
flight
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25
5
10
30
6
4
2
0
0
non-mimetic non-mimetic and
alarm
mimetic alarms
non-mimetic
alarm
mimetic
alarm
honeyeater
alarm
Figure 3. Currawong response to thornbill and honeyeater vocalizations. (a) Mean (+s.e.m.) number of seconds that currawongs (n ¼ 18) delayed feeding at
simulated nests after playback of thornbill vocalizations. Analyses are shown in the electronic supplementary material, table S4. (b) Mean (+s.e.m.) number of
seconds that currawongs (n ¼ 10) feeding in the open spent scanning after playback of thornbill or honeyeater vocalizations; currawongs did not scan the sky
following thornbill song, so this treatment was not included here (electronic supplementary material, figure S3). Pie-charts above bars illustrate the proportion of
currawongs that flew away from the location (black), scanned the sky for more than 1 s (grey) or did not respond with a typical aerial alarm response (white).
Analyses are shown in the electronic supplementary material, table S5.
In support of a deceptive anti-predator function, currawongs
treated all aerial alarms as if they were themselves threatened by
a predator in flight, and the specific benefit of incorporating
mimicry was prolonging this distraction (figure 3a; electronic
supplementary material, video S1). Currawongs were more
likely to scan the sky or flee following either alarm playback
than following song, suggesting that they were deceived by
thornbill alarms (McNemar’s test versus song: non-mimetic
alone: x21 ¼ 15:1, p , 0.001; mixture: x21 ¼ 12:5, p , 0.001;
figure 3a). As a result of distraction, currawongs delayed feeding
8.3 s (+0.4 s.e.m.) longer following non-mimetic aerial alarms
alone than following song (t32 ¼ 5.11, p , 0.0001), and prolonged this delay a further 8 s (+0.9 s.e.m.) if non-mimetic and
mimetic aerial alarm calls were broadcast together (t32 ¼ 2.47,
p ¼ 0.02; figure 3a; electronic supplementary material, table S4).
We found no evidence that thornbill aerial alarms were less
salient to currawongs than aerial alarms of the most frequently
mimicked heterospecific. When foraging in the open, currawongs
scanned the sky for danger following honeyeater alarms, thornbill
non-mimetic alarms and mimetic honeyeater alarms (figure 3b).
There was no difference in the duration of scanning across the
alarm types (linear mixed model effect: F2,13 ¼ 1.91, all p ¼
0.2; figure 3b; electronic supplementary material, table S5).
Two out of 10 currawongs fled to mimetic alarms, but this
was not statistically different compared with real honeyeater
alarms (McNemar’s test: x21 ¼ 0:5, p ¼ 0.5; figure 3b).
4. Discussion
Taken together, our findings demonstrate that brown thornbills
deceive a major nest predator by mimicking alarm calls of other
harmless species. This sophisticated behavioural strategy
exploits the interactions among multiple species across several
trophic levels (figure 1a): thornbills exploit currawong eavesdropping on the salient alarm calls of heterospecifics,
signalling about top predators that are dangerous to all three
species, in order to deceive currawongs into delaying attack
on their nestlings. Given the 40-fold size difference between
thornbills and currawongs, physical attacks by thornbills are
likely to be both ineffective and risky, and deception is perhaps
the only effective defence once a nest is attacked [42].
Although used in the presence of an avian predator, the
aerial alarm calls used by thornbills during nest defence were
deceptive. The alarms were not simply communicating about
danger to mates (e.g. [43]) because they were produced in
the absence of a flying threat—the currawongs were always
stationary on the ground. Indeed, in other circumstances, thornbills produce aerial alarm calls to avian predators in flight and
mobbing alarm calls to stationary avian predators, including
to currawongs [14]. They were also not merely communicating
the presence of danger to offspring [44] because the alarms
were only used once nestlings were already under attack.
Lastly, these aerial alarms are not used in aggressive contexts
by thornbills or the mimicked heterospecifics, and thereby do
not signal aggression [13,45]. Deception is a likely explanation
whenever an alarm signal conveys inaccurate information
about the type, or presence, of danger and in doing so provokes
a response by the predator that benefits the caller but is costly to
the predator [2]. Currawongs indeed treated the alarms as if they
were themselves in danger from above (e.g. [18]). Although predators can pay attention to prey alarms [46,47] and use them to
locate feeding opportunities [48], the use of alarm calls by prey
to fool predators has not been shown previously. This is therefore a novel diversionary display employed by birds during
nest defence, similar to injury feigning and false brooding [49].
A surprising feature of thornbill mimicry is that they
mimicked harmless species rather than dangerous or toxic
ones [4,13]. Unlike many taxa that mimic related or similarly
sized noxious prey, such as the abundant examples of Batesian and Müllerian mimicry among invertebrates, reptiles
and fishes [1,50], the opportunity for such mimicry is rare
for birds. We know of only three cases. The New Guinean
Pitohui and Ifrita genera are toxic, resulting in one case of
Müllerian, and potentially also Batesian, mimicry within Pitohui [51,52]. The nestlings of Laniocera hypopyrra are also
considered to be Batesian mimics of a toxic caterpillar [53].
Finally, burrowing owls mimic rattlesnake sounds to deter
competitors [4]. The absence of noxious models, or difficulties in accurately mimicking vocalizations of much larger
predators, might constrain thornbills into mimicking the
alarm calls of harmless species, which are cues of dangerous
flying predators. Aerial alarms might also signal a more
urgent threat than predator calls because predators are usually
Proc. R. Soc. B 282: 20150798
song
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Ethics. This work was carried out with permission from the Australian
Bird and Bat Banding Scheme, Environment ACT, Australian
National Botanic Gardens and Australian National University
Ethics Committee (B.EEG.06.10).
Data accessibility. Data available from the Dryad Digital Repository:
http://dx.doi.org/10.5061/dryad.fh40b.
Authors’ contributions. B.I. and R.M. conceived the study; B.I., J.M. and
I.L. conducted the study; and all authors contributed to writing.
Competing interests. We have no competing interests.
Funding. This work was supported by an Australian Postgraduate
Award to B.I., the Australian National University, and an Australian
Research Council Discovery Grant (DP0665481) to R.D.M.
Acknowledgements. We thank the Australian National Botanic Gardens
for allowing us access to do our research; Andrew Cockburn, David
Green, Tonya Haff, Helen Osmond, Nicolas and Elodie Magraf, and
Martijn van de Pol for assistance in the field; the Magrath and Shawkey
labs, the EEG reading group, Loeske Kruuk, Andrew Cockburn,
Nick Davies and two anonymous reviewers for comments on the
manuscript; Eben Goodale, David Green, Naomi Langmore,
Amanda Ridley, Graeme Ruxton and many other colleagues for helpful
comments and discussions.
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honeyeater and thornbill alarms broadcast alone, although a
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In summary, we revealed the use of deceptive alarms to
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silent when hunting prey. Demonstrating that dangerous
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that mimicry can confer protection through unexpected mechanisms and expand upon the circumstances in which defensive
mimicry could evolve. Indeed, it is the information conveyed
by the mimetic signal that is important for its function, rather
than any danger posed by the model itself. As mimicry of heterospecific alarm calls is common among songbirds [9,10],
similar protective mechanisms for mimicry may also be
common and requires further investigation.
Aerial alarms caused temporary distraction such that
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There are three potential mechanisms by which including
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identify alarms as deceptive [17]; however, non-mimetic aerial
alarms still caused some distraction, suggesting this is not the
complete explanation. Second, mimicry may enable thornbills
to use alarms that are more salient to currawongs, such as
alarms of larger heterospecifics that are more likely to share
predators with currawongs [58]. Contrary to this hypothesis,
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