Behavioral Ecology

doi:10.1093/beheco/arq221
Advance Access publication 8 February 2011

Original Article

Sound familiar? Acoustic similarity provokes

responses to unfamiliar heterospecific alarm
calls
Pamela M. Fallow, Janet L. Gardner, and Robert D. Magrath
Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National
University, Canberra, ACT 0200, Australia

Eavesdropping on the alarm calls of other species can provide vertebrates with valuable information about danger, and

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often responses to heterospecific calls seem to be acquired through learning. However, animals might not require
learning to respond to heterospecific alarm calls that are acoustically similar to conspecific calls. Although previous work
suggests that learning is necessary for superb fairy-wrens to develop responses to heterospecific alarms, acoustic similarity
might also be important. We tested whether fairy-wrens responded to playback of unfamiliar alarm calls and if the
strength of responses was affected by acoustic similarity to conspecific calls. We then determined which acoustic proper-
ties were likely to be used in alarm call identification. Birds fled to cover after playback of calls that were acoustically
similar to their own but did not usually respond to less similar calls. Fairy-wren aerial alarm calls are high-frequency and
rapidly frequency modulated; their probability of fleeing to playback of unfamiliar calls increased in response to calls with
increasing peak frequencies, and they spent more time in cover following calls with a number of frequency cycles similar
to their own. Fairy-wrens also responded strongly to relatively dissimilar calls of 1 allopatric species, possibly because these
unfamiliar calls resembled those of a sympatric species to which they had learnt to respond. Our study shows that acoustic
similarity can prompt responses to heterospecific alarm calls regardless of experience and together with previous work
suggests that both acoustic similarity and learning are important for interspecific responses to alarm calls. Key words:
Acanthizidae, acoustic structure, alarm calls, interspecific eavesdropping, Maluridae, Malurus cyaneus. [Behav Ecol 22:
401–410 (2011)]

any vertebrates use alarm calls to alert others to the pres-
M ence of danger (Zuberbühler 2009), and heterospecifics
that share the same predators can benefit from responding to
these calls. Alarm calls can convey knowledge about the type
of threat (Seyfarth et al. 1980; Pereira and Macedonia 1991;
Gill and Sealy 2004), the direction from which it is approach-
ing (Evans et al. 1993), how urgent it is (Leavesley and Ma-
grath 2005; Templeton et al. 2005), or a combination of these
types of information (Manser et al. 2002), which help re-
ceivers choose appropriate responses. In addition to warning
conspecifics, other species that are vulnerable to the same
threats can eavesdrop on these calls and gain information
about danger (Sullivan 1984; Fichtel 2004; Randler 2006; Fal-
low and Magrath 2010). Responses to heterospecific alarm
calls have been shown between species within and across ver-
tebrate taxa (Caro 2005): between birds (Hurd 1996; Magrath
et al. 2007; Templeton and Greene 2007), between mammals
(Shriner 1998; Ramakrishnan and Coss 2000; Zuberbühler
2000), a bird responding to a mammal (Rainey et al. 2004),
mammals responding to birds (Randler 2006; Müller and
Manser 2008), and reptiles responding to birds (Vitousek
et al. 2007; Ito and Mori 2010). Heterospecific alarm calls
not only allow eavesdroppers to devote less time to scanning
for danger (Bshary and Noë 1997) but can also provide them
Address correspondence to P.M. Fallow. E-mail: pamela.fallow@anu.
edu.au.
J.L. Gardner is now at Fenner School of Environment and Society, The
Australian National University, Canberra, ACT 0200, Australia
Received 18 August 2010; revised 30 November 2010; accepted 16
December 2010.

The Author 2011. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: journals.permissions@oup.com
with early warnings (Burger 1984), and information that com-
plements that provided by conspecific calls (Nuechterlein
1981; Goodale and Kotagama 2005). The information gained
through interspecific eavesdropping can be so valuable that it
influences the temporary or long-term formation of mixed-
species groups (Goodale et al. 2010).
The advantages of interspecific eavesdropping and its wide-
spread occurrence raise the question of how animals recognize
heterospecific calls as alarm calls. So far, most studies suggest
that responses to heterospecific alarm calls are acquired
through learning. For example, adult bonnet macaques,
Macaca radiata, are better than juveniles at distinguishing het-
erospecific mammalian alarm calls from nonalarms, and anti-
predator responses to playback of heterospecific calls occur
only in macaque populations that have frequent exposure to
those heterospecific calls and therefore the opportunity for
learning (Ramakrishnan and Coss 2000). Similarly, playback
experiments showed that infant vervet monkeys, Cercopithecus
aethiops pygerythrus, exposed more often to alarm calls of su-
perb starlings, Spreo superbus, responded to them at a younger
age potentially by learning from the behavior of other group
members (Hauser 1988). Some species respond to heterospe-
cific alarm calls that are acoustically dissimilar to conspecific
calls (Shriner 1998; Magrath et al. 2009a, 2009b), or even
when they do not have calls of their own (Griffin et al.
2005; Vitousek et al. 2007; Ito and Mori 2010), suggesting that
acoustic similarity to conspecific calls is not a requirement of
responding to heterospecific calls. Finally, the most direct
demonstration to date that animals can learn to respond to
alarm sounds is shown in golden-mantled squirrels, Spermophi-
lus lateralis, which can learn to associate a novel sound with the
402
appearance of a model predator (Shriner 1999). Thus, various
studies using different experimental methods provide both
direct and indirect evidence of the importance of learning
for the development of adaptive responses to heterospecific
alarm calls.
Although learning appears to be important for interspecific
responses to alarm calls, vertebrates might not require learning
to respond to heterospecific calls if they can identify them
based solely on their acoustic structure. Unlike other signals,
such as those used in courtship, that are directed solely at
conspecifics, alarm calls do not need to be species-specific
and so the calls of sympatric species can share similarities with-
out reducing effectiveness (Marler 1957). Therefore, alarm
calls of different species can be acoustically similar as a result
of calls retaining features from a common ancestor (de Kort
and ten Cate 2001) or convergence in acoustic structure (dis-
cussed below), thus provoking interspecific responses. Birds
can have an innate disposition to respond to conspecific alarm
calls (Davies et al. 2004) and might respond to unfamiliar
alarm calls because they are acoustically similar to their own
(McCracken and Sheldon 1997; de Kort and ten Cate 2001;
Ghirlanda and Enquist 2003). For example, Australian apostle-
birds, Struthidea cinerea, responded to playback of a North
American Carolina wren, Thryothorus ludovicianus, mobbing call
despite having no opportunity to learn it (Johnson et al. 2003),
implying the importance of acoustic similarity for prompting
responses to unfamiliar alarm calls (Johnson et al. 2003). Thus,
animals might not need to experience alarm calls that are
acoustically similar to their own, and recognition of heterospe-
cific calls may be enabled by acoustic similarities between the
calls of different species. However, there have been no playback
experiments using a range of alarm calls varying in their degree
of acoustic similarity to calls of the receiving species. As a result,
it is unknown whether vertebrates respond similarly to all het-
erospecific calls that they identify as alarm calls or if the
strength of responses is affected by acoustic similarity to con-
specific calls.
The design of alarm calls reflects their function as a signal
and their efficacy in a particular context, and so the calls of
different species can be acoustically similar as a result of con-
vergence on the most effective design for a particular environ-
ment (Marler 1955; Russ et al. 2004). Alarm calls have 2
common designs depending on their function: ‘‘mobbing’’
alarm calls attract others to join the caller in harassing a pred-
ator that poses little immediate danger and so are typically
relatively low-frequency broadband calls that are repeated
over a period of time, allowing calls to be locatable to both
the predator and other prey, and attracting more receivers to
the source of the call (Hurd 1996; Bradbury and Vehrencamp
1998). Conversely, ‘‘flee’’ alarm calls, such as aerial alarm calls
produced in response to predators in flight, signal the need to
immediately freeze or escape to cover, and are typically
high-frequency and short in duration, making the call difficult
to overhear and perhaps difficult to locate (Bradbury and
Vehrencamp 1998; Jurisevic and Sanderson 1998). Interspe-
cific responses to alarm calls might therefore occur as a result
of the calls of different species converging on broadly similar
acoustic structures.
Superb fairy-wrens, Malurus cyaneus, seem to require expe-
rience to recognize at least some heterospecific alarm calls.
When living sympatrically with white-browed scrubwrens, Ser-
icornis frontalis, they usually respond to playback of scrubwren
aerial alarm calls by immediately fleeing to cover (Magrath
et al. 2007). However, a population of fairy-wrens living in
the absence of scrubwrens did not respond to playback of
scrubwren calls, despite the calls of these 2 species
overlapping in frequency, being of similar duration and both
featuring rapid frequency modulation (Magrath et al. 2009b).
Behavioral Ecology
This suggests that fairy-wrens are capable of high levels of
acoustic discrimination and that the acoustic similarity be-
tween these calls and conspecific calls does not prompt re-
sponses to scrubwren calls without experience. Playback
experiments also show that fairy-wrens flee in response to
acoustically very dissimilar alarm calls of sympatric New Hol-
land honeyeaters, Phylidonyris novaehollandiae, (Magrath et al.
2009a), showing that call similarity is not essential for re-
sponse and again implying learning. Furthermore, fairy-wrens
usually did not respond to honeyeater calls played back in
reverse despite the fact that reversed calls had almost all of
the same acoustic properties as ‘‘normal’’ honeyeater calls
(Magrath et al. 2009b). This implies that fairy-wrens learn to
respond to the very specific acoustic structure of normal hon-
eyeater calls. However, although it is likely that scrubwren calls
are the most acoustically similar heterospecific calls to those
of fairy-wrens in Canberra (Magrath et al. 2009b), fairy-wrens
may not require experience to respond to heterospecific calls
that are even more similar to their own calls than those of
scrubwrens, such as those of closely related species.
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We investigated whether experience was necessary for fairy-
wrens to respond to unfamiliar heterospecific alarm calls and
specifically if a greater degree of acoustic similarity to conspe-
cific calls increased the strength of responses. We then ana-
lyzed whether particular acoustic properties of these
unfamiliar calls were likely to have affected fairy-wren
responses.
METHODS
Study area and species
We studied superb fairy-wrens around Lake Burley Griffin and
in the Australian National Botanic Gardens (lat 3516#S, long
1496#E) in Canberra, Australia. Fairy-wren groups living in
the Botanic Gardens were identified by the inclusion of color-
banded birds, whereas groups by the lake were distinguished
by location. Territories within the Botanic Gardens have
a mean width of around 80 m (Mulder 1995) and, on a single
day, groups sampled within and outside the Gardens were
found at least 100 m apart. Fairy-wrens breed cooperatively,
with groups typically consisting of a dominant pair that may
be assisted by up to several subordinate males (Cockburn et al.
2003). They forage for invertebrates primarily on the ground
and frequently venture out of cover and into open areas. Each
fairy-wren group defends its territory during the breeding
season until the cooler months when territories break down,
and neighboring groups gather to form larger flocks that
commonly include other species (Bell 1980, Fallow PM, per-
sonal observation).
Fairy-wrens signal the presence of predatory birds in flight by
producing aerial alarm calls consisting of one or more high-fre-
quency elements. Each element consists of a single band that is
rapidly frequency modulated about a constant carrier fre-
quency (mean peak frequency: 9.1 kHz, frequency range: 8–
11 kHz, Magrath et al. 2007). Calls contain more elements
and have a higher maximum frequency when threats are
closer, and fairy-wrens typically respond in a 2-stage process
by 1) immediately fleeing to cover; and 2) waiting in cover
before reemerging, with the amount of time spent in cover
increasing as the number of elements in the call increases
(Fallow and Magrath 2010). In Canberra, fairy-wrens are vul-
nerable to predatory birds including pied currawongs, Strepera
graculina; grey butcherbirds, Cracticus torquatus; laughing koo-
kaburras, Dacelo novaeguinea; and collared sparrowhawks,
Accipiter cirrocephalus (Magrath et al. 2009b).
To test the response of fairy-wrens to unfamiliar calls with
varying degrees of acoustic similarity to conspecific calls, we
 Fallow et al. • Acoustic similarity provokes responses to alarm calls 403

presented them with alarm calls from 7 allopatric species in
the same families as superb fairy-wrens and white-browed
scrubwrens. The allopatric species included 3 congeneric spe-
cies in the family Maluridae: splendid fairy-wren, Malurus
splendens; variegated fairy-wren, M. lamberti; and white-winged
fairy-wren, M. leucopterus; and 4 species in the family Acanthi-
zidae: brown gerygone, Gerygone mouki; chestnut-rumped
thornbill, Acanthiza uropygialis; western thornbill, A. inornata;
and southern whiteface, Aphelocephala leucopsis.
The superb fairy-wren is a sedentary species (Higgins et al.
2001), and individuals in our study population were therefore
highly unlikely to have experienced calls of the allopatric spe-
cies used in the playback experiment. However, in other areas
of Australia, the geographic range of superb fairy-wrens over-
laps with that of most of the playback species. Superb fairy-
wrens are widespread in south-eastern Australia, so that some
areas of its range overlap with splendid fairy-wrens and varie-
gated fairy-wrens (South Australia, inland Victoria, New South
Wales, and southern Queensland), white-winged fairy-wrens
(South Australia, northern Victoria, New South Wales, and
brown gerygone, Batemans Bay, New South Wales; chestnut-
rumped thornbill and southern whiteface, Nallan Station,
Western Australia; and western thornbill, Flint State Forest,
Western Australia. All calls from allopatric species were pro-
voked using a gliding life-sized model of the collared sparrow-
hawk because, unlike currawongs, they occur throughout
Australia. Alarm calls prompted by the currawong and spar-
rowhawk models are acoustically indistinguishable from each
other and from calls prompted by real predators (Magrath
et al. 2007), and birds respond to playback of calls prompted
by models in the same way as playback of calls prompted by
live predators (Leavesley and Magrath 2005; Magrath et al.
2007). The calls of all species were recorded on dry days with
low wind. While one person launched the model by hand,
another recorded calls from a distance of 2–6 m from the
group or individual using a Sennheiser ME66 directional mi-
crophone and a Marantz PMD670 digital recorder, sampling
wave files at 44.1 kHz and 16 bits. Prior to each model pre-
sentation, we observed the behavior of the group for 5 min
and did not attempt to launch models if alarm calls were given

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inland Queensland), brown gerygones (eastern coast of Vic-
toria, New South Wales, and coastal Queensland), and chest-
nut-rumped thornbills and southern whitefaces (South
Australia, Victoria, New South Wales, and inland Queensland,
Barrett et al. 2003). The only playback species with
a geographic range that has no overlap with that of superb
fairy-wrens is the western thornbill, which is restricted to the
southwestern corner of Western Australia. Superb fairy-wrens
are the only malurid species commonly found in our study site
in Canberra (Fennell 2009), where the only other playback
species recorded, brown gerygones, are rare visitors and have
not been sighted for several years (Overs 2009).
Recording alarm calls
We recorded aerial alarm calls from superb fairy-wrens in the
Botanic Gardens over a period of 7 weeks during May and June
2008, with calls provoked using a gliding, life-sized model of
the pied currawong (see Magrath et al. 2007 for model spec-
ification). Calls from the allopatric species were recorded in
various locations around Australia during 2006 and 2007:
splendid fairy-wren, Perth, Western Australia; variegated and
white-winged fairy-wrens, Guilderton, Western Australia;
during observation or if any potentially threatening species
were seen nearby. This ensured that we recorded alarm calls
provoked by the model predator and not by other stimuli.
Acoustic analyses
We cropped digital recordings in Cool Edit Pro v. 1.2a (Syntril-
lium Software, Phoenix, AZ) to isolate the aerial alarm calls,
leaving several seconds of background noise prior to the mod-
el’s release and following its landing. We used Raven Pro 1.3
(Charif et al. 2008) to generate spectrograms using a Black-
man window function, a temporal grid resolution of 0.295 ms
with 94.9% overlap and a frequency grid resolution of 86.1
Hz. As alarm calls were recorded from different bird groups,
each call was likely to be produced by a different individual.
We randomly selected one element from calls featuring a high
signal-to-noise ratio, minimal reverberation, and no overlap-
ping background sounds, leaving us with a sample of unique
high-quality elements for each species (Table 1; Figure 1). We
then defined a range selection around each element on the
spectrogram and measured the following acoustic properties:
maximum frequency (kilohertz), minimum frequency
(kilohertz), peak frequency (the frequency at greatest

Table 1
Comparison of call elements of birds in this study

Frequency
Peak frequency Frequency range Element duration Number of cycles modulation rate
Species N (kHz) mean 6 SD (kHz) mean 6 SD (ms) mean 6 SD mean 6 SD (Hz) mean 6 SD

Family Maluridae
Superb fairy-wren 12 9.1 6 0.34 2.2 6 0.35 90.4 6 18.8 7.7 6 1.5 105.2 6 8.0
Splendid fairy-wren 12 8.9 6 0.25 1.8 6 0.29 80.7 6 16.1 7.5 6 1.3 107.7 6 10.0
Variegated fairy-wren 12 8.9 6 0.40 2.1 6 0.31 79.9 6 10.4 8.1 6 1.1 114.3 6 9.2
White-winged fairy-wren 12 9.2 6 0.31 1.8 6 0.55 73.9 6 27.4 — —
Family Acanthizidae
Brown gerygone 12 6.5 6 0.56 2.3 6 0.29 50.5 6 10.6 3.9 6 1.2 129.7 6 10.3
Western thornbill 12 8.3 6 0.50 2.7 6 0.57 64.3 6 15.0 — —
Southern whiteface 12 6.7 6 0.22 1.6 6 0.14 40.6 6 13.2 — —
Chestnut-rumped thornbill 12 6.8 6 0.35 1.5 6 0.48 91.4 6 50.1 — —
White-browed scrubwrena 7 7.8 6 1.00 3.0 6 0.56 83.0 6 16.8 6.8 6 1.9 105.5 6 7.9
Buff-rumped thornbilla 13 8.3 6 0.56 2.4 6 0.45 80.6 6 23.6 — —
Family Psittacidae
Crimson rosella (control)b 12 2.6 6 0.52 1.2 6 0.61 132.0 6 100.3 — —

a
Species living in sympatry with superb fairy-wrens in Canberra, examined in the ‘‘DISCUSSION.’’ b Measurements were taken from the loudest
element in the call.
404 Behavioral Ecology

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Figure 1
Spectrograms of aerial alarm call elements of superb fairy-wrens, the allopatric species used in the playback experiment, and the sympatric
species examined in the ‘‘DISCUSSION.’’ Elements presented have measurements within 1 SD of the mean values for each species’ maximum
frequency (kilohertz), minimum frequency (kilohertz), element duration (milliseconds) and where applicable, frequency modulation rate
(hertz). Spectrograms were produced in Raven Pro 1.3 using settings as described under ‘‘METHODS’’ for Acoustic analyses.

amplitude, kilohertz), frequency range (kilohertz), element
duration (milliseconds), number of frequency cycles, and fre-
quency modulation rate (number of frequency cycles per sec-
ond, hertz). Measurements were taken from the entire
element at the same scale on the screen and with standard
spectral settings.
Playback experiment
The playback experiment aimed to test how superb fairy-wrens
responded to unfamiliar aerial alarm calls that varied in their
degree of acoustic similarity to conspecific calls. If the response
of fairy-wrens to playback of the heterospecific calls varied in
strength according to the degree of acoustic similarity, it would
indicate that similarity could provoke responses to heterospe-
cific alarm calls. We composed playbacks from high-quality ele-
ments chosen from the natural calls of 9 species: splendid
fairy-wrens, variegated fairy-wrens, white-winged fairy-wrens,
brown gerygones, chestnut-rumped thornbills, western thorn-
bills, and southern whitefaces. Superb fairy-wren alarm calls
were used as a positive control, and the piping or ‘‘bell’’ calls
(Higgins 1999; Magrath et al. 2007) of crimson rosellas,
Platycercus elegans, harmless parrots that live sympatrically with
fairy-wrens in Canberra, were used as a negative control
(Table 1).
We prepared 12 playback calls for each species, composing
each call from a unique element to avoid pseudoreplication of
calls. Elements were selected from different recordings or from
calls of 2 different birds in the same recording when there
were fewer than 12 recordings for a species. We filtered out all
sound below 4 kHz in the passerine alarm calls and all sound
below 2 kHz in the rosella control calls. Previous work has
shown that superb fairy-wren aerial alarm calls containing 4
elements signal urgent danger, and fairy-wrens respond by
fleeing to cover in 100% of cases (Fallow and Magrath
2010). Therefore, we constructed 4-element passerine alarm
calls so that it would be clear whether they responded to
the playbacks. Each alarm call was constructed by pasting
Fallow et al. • Acoustic similarity provokes responses to alarm calls 405

the same element 4 times, with a 45 ms interval between the
end of each element and the start of the next element. This
standard interval length was within the natural range of alarm
calls used to generate playbacks and ensured that differences
in fairy-wren responses to playback were due only to variation
in the element structure of different species and not interval
length.
Playbacks were uncompressed wave files broadcast from
a Roland Edirol R-09 HR solid-state playback and recording
device (20–22 000 Hz) via a Kemo Electronics integrated am-
plifier (20–25 000 Hz) and a Response Dome tweeter speaker
(1500–20 000 Hz). Playback amplitude was measured in Raven
Pro 1.3 and calibrated against a tone that had its amplitude
determined using a digital level meter. The playback equip-
ment was mounted around the observer’s waist and playbacks
broadcast at an element amplitude of 61 dB at 5 m, which is
around 1 standard deviation (SD) above the mean amplitude
for superb fairy-wrens (Magrath et al. 2007), to ensure that
playbacks were audible. We played back calls from the 9 spe-
cies to 108 fairy-wren groups in Canberra in June and July
detect an effect on the amount of time fairy-wrens spent in
cover after fleeing (using only playback calls that provoked
birds to spend time in cover, n ¼ 53).
We then tested whether specific acoustic properties influ-
enced antipredator responses. A GLM with binomial error
was used to analyze the binary responses (stay or flee), and
a GLM with a normal distribution to analyze variation in the
amount of time fairy-wrens spent in cover. Both GLMs were
fitted with the following acoustic variables: peak frequency
(kilohertz), element duration (milliseconds), and number
of frequency cycles. Variables measured in kilohertz were log
transformed. We used the Wald statistic to test for fixed effects
then sequentially removed nonsignificant terms one by one
until only significant effects remained. Analyses were per-
formed using GenStat Software v. 11 (VSN International
Ltd., Hemel Hempstead, UK.) with significance levels set at
P , 0.05.
RESULTS

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2009. Playback calls were grouped into 12 sets of 9 calls, in- Acoustic similarity of calls from different species
cluding one call from each species. Playback sets were then
There was substantial variation in the acoustic similarity of
presented one at a time, with each completed within a single
alarm calls from the allopatric playback species to those of su-
day. Each playback call was presented to a different fairy-wren
perb fairy-wrens (Table 1; Figure 1). The canonical variates
group, and calls were presented in random order. Prior to
plot provided a 2D representation of acoustic similarity be-
each playback, the fairy-wren group was observed for 5 min
tween the calls of different species, with the 3 acoustic prop-
to ensure that birds were not agitated by conspecifics or the
erties explaining a total of 98.7% of variation between
observer and that no threatening species or other bird species
measurements taken from the calls of the 8 playback species
that could provide cues of danger were nearby (,10 m). If no
(Figure 2). The degree of acoustic similarity between calls was
alarm calls were detected during the observation period, the
represented by distance on the x axis (canonical variate 1),
playback was presented to a randomly chosen focal bird when
it was foraging on the ground at least 50 cm from cover. We
presented playbacks from a distance of around 8 m (mean 6
SD ¼ 8.21 6 0.91) from the focal bird and recorded one of
the following immediate responses: 0, no response; 1, scan; 2,
scan then flee; and 3, immediately flee to cover or away from
their original position. These graded responses were then
sorted into binomial responses for comparison with previous
studies: 0, nonflee (0, 1, and 2) and 1, flee (3). If the focal
bird fled to cover, the duration of time spent in cover (sec-
onds) before it emerged was recorded if possible but capped
at 60 s. To minimize stress caused to the birds, we provoked
alarm calls from different fairy-wren groups when recording
calls and during the playback experiment presented each
group with only 1 alarm call.

Statistical analyses
To compare the acoustic similarity of superb fairy-wren alarm
calls to those of the allopatric species used in the playback ex-
periment, we generated a canonical variates plot using acous-
tic measurements taken from aerial alarm calls of the 8
species. Calls were placed on a 2D plane according to the
amount of variation explained by: peak frequency (kilohertz),
element duration (milliseconds), and number of frequency
cycles. Peak frequency was log transformed. We chose these
variables to classify calls because they were not correlated with
each other. Minimum, maximum, and peak frequencies were
particularly highly correlated, and we used peak frequency Figure 2
because it was easiest to measure and the most repeatable. Canonical variates plot of aerial alarm calls of the species used in the
Using intergroup distances from the canonical variates plot playback experiment. In order from most to least similar to superb
as a proxy for acoustic similarity between calls, we then used fairy-wrens according to intergroup distances, these are superb fairy-
wren (:), splendid fairy-wren (1), variegated fairy-wren (h), brown
generalized linear models (GLMs) to test whether there was
gerygone (d), white-winged fairy-wren (n), western thornbill (s),
a relationship between acoustic similarity to superb fairy-wren southern whiteface ( ), and chestnut-rumped thornbill (e). Circles
calls and the strength of fairy-wren responses to playback. A represent confidence regions around mean values for each species’
GLM with binomial error was used to detect an effect of calls calculated using the following acoustic properties: peak
intergroup distance on the binary responses (stay or flee, frequency (kilohertz), element duration (milliseconds), and number
n ¼ 96)), and a GLM with a normal distribution was used to of frequency cycles.
406 Behavioral Ecology

which explained 75.3% of variation, and by distance on the y

axis (canonical variate 2), which explained 23.3% of variation.
Loadings in the plot of calls used in the playback experiment
were canonical variate 1 (peak frequency, 218.3; element du-
ration, 8.7; and number of cycles, 21.1) and canonical variate
2 (peak frequency, 242.0; element duration, 29.8; and num-
ber of cycles, 0.5).
Superb fairy-wren aerial alarm calls were more similar to
those of most of its congeners than to the calls of species in
the family Acanthizidae. Calls of most of the malurids were
clustered together, indicating high acoustic similarity within
the genus. The calls of white-winged fairy-wrens were separated
from those of the other malurids due to their lack of frequency
modulation (no frequency cycles). Calls of the acanthizids
were more variable than those of the malurids and so more
spread out. We used intergroup distances between the mean
values for calls of each playback species to estimate their de-
gree of acoustic similarity relative to superb fairy-wren calls.
Calls of the allopatric playback species in order from most to
least acoustically similar to superb fairy-wren calls with their

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intergroup distances were 1) splendid fairy-wren, 0.64; 2) var-
iegated fairy-wren, 0.75; 3) brown gerygone, 7.93; 4) white-
winged fairy-wren 8.84; 5) western thornbill, 8.88; 6) southern
whiteface, 10.42; and 7) chestnut-rumped thornbill, 10.59.

Fairy-wren responses to unfamiliar calls

Fairy-wrens responded more strongly to playback of unfamiliar
calls with greater acoustic similarity to conspecific calls. Play-
back calls with lower intergroup distances to fairy-wren calls
provoked more fairy-wrens to flee to cover (GLM: v21 ¼ 16:79;
P , 0.001; Figure 3a) and to spend more time in cover after
fleeing (GLM: v21 ¼ 19:16; P , 0.001; Figure 3b). Fairy-wrens
always fled to cover after playback of conspecific calls (positive
control), to most calls of other malurids, and to 75% of calls
from western thornbills. However, they fled to only one brown
gerygone call and did not flee to playback of southern white-
face or chestnut-rumped thornbill calls (Figure 4a). Playback
of rosella calls (negative control) never elicited flight or even
a vigilance response in fairy-wrens.
Although superb fairy-wrens had a high probability of flee-
ing to playback of calls of congeners and western thornbills, the
amount of time they spent in cover differed among species
(analysis of variance excluding birds that did not flee or that
fled to a location outside of cover, F4,48 ¼ 6.79, P , 0.001;
Figure 4b). Fairy-wrens spent 16 6 8.6 s in cover (mean 6 SD)
after playback of conspecific calls, results practically identical
to those found in a previous study (mean 6 SD ¼ 16 6 5.2 s,
Fallow and Magrath 2010). Their response to playback of
splendid fairy-wren calls was no different to their response
to conspecific calls (mean difference 6 least significant dif-
ference at 5% ¼ 0.8 6 5.1 s); they always fled to splendid fairy-
wren calls and then spent the same amount of time in cover
(mean 6 SD ¼ 15.1 6 8.1 s). However, fairy-wrens spent less
time in cover after fleeing to playback of calls of other heter-
ospecifics (mean difference 6 least significant difference at
5%): variegated fairy-wren (7.9 6 5.2 s); white-winged fairy-
wren (9.0 6 5.5 s); and western thornbill (10.8 6 5.5 s).
In all cases where superb fairy-wrens did not flee in response
to playback of a malurid call, they responded with an increase
in vigilance, such as raising the head and scanning (Figure 4a).
Scanning was also seen in 2/11 cases when they did not flee to
playback of brown gerygone calls and in 1/3 cases when they
did not flee to playback of western thornbill calls. Also, de-
spite not fleeing to any playbacks of calls of southern white-
faces and chestnut-rumped thornbills, fairy-wrens responded
with scanning in 1 and 2 cases, respectively.
Figure 3
Relationships between the intergroup distance of each playback
species’ calls to superb fairy-wren calls and fairy-wren responses to
playback: (a) the proportion of focal birds immediately fleeing and
(b) the mean duration of time spent in cover before reemerging
(seconds). Playback species were: Superb fairy-wren (:), splendid
fairy-wren (1), variegated fairy-wren (h), brown gerygone (d),
white-winged fairy-wren (n), western thornbill (s), southern
whiteface ( ), and chestnut-rumped thornbill (e).
Acoustic properties influencing responses
Only 2 acoustic properties affected fairy-wren responses to play-
back, with each property influencing different antipredator be-
haviors. The probability of fairy-wrens fleeing to cover was
greater in response to playback of calls with higher peak frequen-
cies (GLM: v21 ¼ 31:90; P , 0.001), and the amount of time
spent in cover increased following playback of calls with a greater
number of frequency cycles (GLM: v21 ¼ 11:94; P ¼ 0.001). The
substitution of frequency modulation rate for the number of
frequency cycles made no difference to the outcome, whether
it was treated as a continuous variable (GLM:v21 ¼ 11:48;
P ¼ 0.001) or as a categorical variable (GLM with frequency
modulation as present or absent:v21 ¼ 12:46; P , 0.001).
DISCUSSION
Our study supports the suggestion by Marler (1957) that ver-
tebrates will respond to heterospecific alarm calls if they are
acoustically similar to conspecific calls. Superb fairy-wrens re-
sponded more strongly to unfamiliar calls that were acousti-
cally more similar to conspecific alarm calls. This shows how
birds can respond to alarm calls of congeners despite having
Fallow et al. • Acoustic similarity provokes responses to alarm calls
Figure 4
The observed responses of superb fairy-wrens to playback of
unfamiliar 4-element aerial alarm calls: (a) the proportion of focal
birds fleeing to cover or scanning; and (b) the mean (1 standard
error) duration of time (seconds) the focal bird spent in cover before
reemerging. Playback calls are presented from left to right in order of
acoustic similarity to superb fairy-wren calls based on intergroup
distances calculated by the canonical variates plot of playback species
(Figure 2). Mean values for the acoustic properties affecting the
probability of fleeing, and the amount of time spent in cover are
presented for each species. Superb fairy-wren alarm calls served as
a positive control. Playback of crimson rosella piping calls, the
negative control, did not elicit any response and are not represented
here.
no experience of them. Responding to acoustic similarity is
likely to benefit fairy-wrens in the large areas where their geo-
graphic range overlaps with that of other malurid species,
which themselves probably also respond to calls of congeners,
including superb fairy-wrens.
Fairy-wrens responded to calls that were acoustically similar
to their own, with the strength of response increasing with in-
creasing similarity. This suggests that they generalize responses
from conspecific calls to unfamiliar calls that are acoustically
similar (Ghirlanda and Enquist 2003). All playback calls had
the same amplitude, tempo, and number of elements, and so
variation in the responses they provoked were due to differ-
ences in the acoustic structure of elements. Therefore, fairy-
wrens do not require learning to respond to heterospecific
calls that are acoustically similar to their own, including those
of congeners.
Fairy-wren responses to playback were affected by specific
acoustic properties and how similar they were to conspecific
calls. Fairy-wrens had a higher probability of fleeing to calls
with high peak frequencies and then spent more time in cover
when calls had a number of frequency cycles similar to their
own calls. The species-specificity of calls and responses to them
407
can be attributed to specific acoustic properties or to combina-
tions of acoustic properties they contain (Brémond 1976; de
Kort and ten Cate 2001). Peak frequency and the number of
frequency cycles appeared to be the key acoustic properties
affecting fairy-wren responses to heterospecific alarm calls.
This offers proximate reasons for why fairy-wrens fled to the
unfamiliar calls of some species but not to others: the calls of
malurids and western thornbills had higher peak frequencies
than most of the acanthizids and apparently therefore re-
sulted in a higher probability of birds fleeing to these calls.
Additionally, although brown gerygone calls had about the
same amount of overall similarity to superb fairy-wren calls
as those of white-winged fairy-wrens (Figure 2), the low peak
frequency of gerygone calls appears to explain why fairy-wrens
usually did not flee to playback of these calls and yet fled to
most calls of white-winged fairy-wrens. Gerygone calls had the
lowest peak frequencies of all species in the playback experi-
ment, whereas the peak frequency of white-winged fairy-wren
calls was close to that of its congeners. Peak frequency might
also be used to identify alarm calls because it is relatively re-
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sistant to degradation. Our conclusions are limited to the
amount of variation in the natural calls of the species we
examined and the acoustic properties that we measured. To
confirm that fairy-wrens base their responses on these partic-
ular acoustic properties, and how variation in these properties
can affect responses, we need additional experiments testing
the effect of varying specific acoustic properties while keeping
all other parameters constant.
Superb fairy-wrens responded cautiously to unfamiliar alarm
calls by varying their behavior in 2 separate stages. They ap-
peared to process calls in at least 2 steps to produce appro-
priate responses: 1) rapidly decide whether to flee or not,
depending on whether the peak frequency of a call was in
the range of a conspecific call; and 2) once in the safety of
cover, decide how likely the call was a false alarm based on the
number of frequency cycles and consequently how much time
to spend in cover before reemerging. For example, fairy-wrens
had a high probability of fleeing to playback of all malurid
calls because they all had high peak frequencies, but they
spent less time in cover after variegated and white-winged
fairy-wren calls because, unlike splendid fairy-wrens calls,
these calls did not have a number of frequency cycles similar
to that of conspecific calls. This cautious initial response fol-
lowed by a second stage of escape behavior is comparable with
the response of western grebes, Aechmophorus occidentalis, to
playback of alarm calls by Forster’s terns, Sterna forsteri: after
playback, most grebes either assumed an alarmed posture or
left the nest, but on no occasion did playbacks provoke the
full alarm response of diving into the water, presumably be-
cause grebes rely on further information in the form of visual
cues (Nuechterlein 1981). A 2-stage response process allows
fairy-wrens to increase their level of safety in response to sig-
nals that might indicate urgent danger while reducing the
amount of time wasted in cover after false alarms. The re-
sponses of fairy-wrens to playback of unfamiliar heterospecific
alarm calls lends support to a previous study, which suggested
that they varied the amount of time spent in cover in response
to the degree of urgency in conspecific calls: although fairy-
wrens fled to playback of all multielement conspecific calls,
the amount of time spent in cover increased with an increas-
ing number of elements in the call, suggesting the assessment
of danger (Fallow and Magrath 2010).
The stronger responses of superb fairy-wrens to playback
of calls of congeners with increasing phylogenetic related-
ness appear to be due to the calls of more closely related spe-
cies being acoustically more similar. Superb fairy-wrens are
the sister species to splendid fairy-wrens, intermediately re-
lated to variegated fairy-wrens, and most distantly related to
408
white-winged fairy-wrens (Gardner et al. 2010), and the de-
gree of relatedness between superb fairy-wrens and its con-
geners corresponded roughly with both the degree of
acoustic similarity between calls and the strength of re-
sponses to playback. An increase in response strength with
increasing phylogenetic relatedness was also shown by the
responses of 2 turtle dove species, Streptopelia roseogrisea and
S. vinacea, to playback of heterospecific ‘‘perch-coos,’’ long-
range territorial vocalizations; both species called more in
response to sister species than to the calls of more distantly
related congeners (de Kort and ten Cate 2001). If the
acoustic similarity of alarm calls is a result of phylogeny
then the degree of relatedness may have affected fairy-wren
responses through changes in acoustic properties, such as
the number of frequency cycles. Otherwise, it is also possi-
ble that phylogeny affected responses through variation in
acoustic features that we did not measure. Therefore, fu-
ture studies should consider controlling for effects of phy-
logenetic distance either by using synthetic calls or the calls
of species with a similar degree of relatedness.
The importance of acoustic similarity in allowing fairy-wrens
to respond to unfamiliar calls might explain why fairy-wrens
did not respond to the apparently similar calls of white-browed
scrubwrens and yet responded strongly to the relatively dissim-
ilar calls of western thornbills. Although fairy-wrens in our
study site respond strongly to scrubwren calls (Magrath
et al. 2007; Fallow and Magrath 2010), a population of fairy-
wrens living in the absence of scrubwrens did not respond to
playback of scrubwren calls indicating urgent danger
(Magrath et al. 2009b), implying that learning is a prerequisite
for fairy-wrens to respond to these calls. However, fairy-wrens
in our study responded strongly to the unfamiliar calls of
western thornbills, calls that are generally less similar to
fairy-wren calls then those of scrubwrens. Western thornbills
were the only acanthizid species with calls provoking strong
responses, possibly because their calls have a relatively high
peak frequency or because fairy-wrens in our study site were
influenced by experience with the acoustically similar calls of
a sympatric species. Fairy-wrens in Canberra live sympatrically
with buff-rumped thornbills, Acanthiza reguloides, a species that
is closely related to western thornbills and so might have sim-
ilar calls. We generated a second canonical variates plot in-
cluding calls of white-browed scrubwrens and buff-rumped
thornbills to see how similar the calls of these sympatric spe-
cies were to those of fairy-wrens and the allopatric species
used in the playback experiment. The plot suggested that
scrubwren calls were generally quite similar to fairy-wren calls
(intergroup distance to fairy-wren calls: 2.9). However, the
peak frequency of scrubwren calls (7.8 kHz) might be too
low to prompt fairy-wrens to flee to them without experience.
Although buff-rumped thornbill calls were generally quite dis-
similar to fairy-wren calls, they were indistinguishable from
western thornbill calls (intergroup distance to superb fairy-
wren calls: western thornbill, 9.13; buff-rumped thornbill,
9.31). Therefore, we consider it likely that fairy-wrens in Can-
berra learnt to respond to calls of sympatric buff-rumped
thornbills and then generalized responses to calls of allopatric
western thornbills because they are acoustically similar (Ghir-
landa and Enquist 2003). Fairy-wrens are known to respond to
the acoustically dissimilar calls of sympatric heterospecifics;
for example, they respond to aerial alarm calls of New Hol-
land honeyeaters (Melphagidae), which are low frequency
with a monotonic decline in frequency over time (Magrath
et al. 2009b). If fairy-wrens in our study site fled to playback of
western thornbill calls because they were similar to calls they
had learnt, this would be an example of a receiver bias gen-
erated through learning (ten Cate and Rowe 2007). Learning-
based bias differs from a neural template, where there is an
Behavioral Ecology
innate response to stimuli, such as conspecific calls (Davies
et al. 2004), as it allows animals to generalize responses to
novel stimuli that resemble stimuli to which they have learnt
to respond (Ghirlanda and Enquist 2003).
In addition to provoking responses to unfamiliar alarm calls
that are highly similar to conspecific alarm calls, acoustic sim-
ilarity might make heterospecific calls easier to learn to recog-
nize (Magrath et al. 2009b). Fairy-wrens that did not flee to
playback of the dissimilar calls of acanthizids usually showed
no change in behavior, but in all 3 cases when birds did not
flee to playback of similar calls of congeners, they still re-
sponded by scanning. If unfamiliar heterospecific alarm calls
have some degree of acoustic similarity to conspecific calls,
they might provoke vigilance in individuals that have not
learnt to associate it with danger. An example of this can be
seen in the response of ringtailed lemurs, Lemur catta, to play-
back of alarm calls from Verreux’s sifakas, Propithecus verreuxi:
wild lemurs live in sympatry with sifakas in Madagascar and
respond appropriately to sifaka calls indicating aerial or ter-
restrial predators. Although a colony of lemurs born in Japan
Downloaded from http://beheco.oxfordjournals.org/ by guest on July 8, 2014
had no experience of sifaka calls and did not respond appro-
priately to sifaka calls indicating different predator types,
some individuals nevertheless responded to the unfamiliar
heterospecific calls by looking up (Oda and Masataka 1996).
In another example, chicks of the common cuckoo, Cuculus
canorus, which parasitizes the nests of reed warblers, Acrocepha-
lus scirpaceus, have an innate response to alarm calls used by
parent warblers to warn nestlings of danger and suppress beg-
ging calls but require experience to develop appropriate re-
sponses. Cuckoo chicks that were raised by other host species
responded only to warbler alarm calls but by inappropriately
increasing their begging rate (Davies et al. 2006). In cases
such as these, where there is a weak or incorrect innate re-
sponse to heterospecific alarm calls, experience is required
for the development and refinement of appropriate responses
(Magrath et al. 2010).
In conclusion, responding to sounds that are acoustically sim-
ilar to conspecific alarm calls can allow birds to respond to het-
erospecific calls without having to learn them. In addition to
learning responses, this shows how vertebrates can distinguish
relevant signals from the plethora of sounds in the acoustic en-
vironment. Furthermore, because the calls of different species
can converge on similar acoustic structures, acoustic similarity
may be as widespread as learning in allowing vertebrates to re-
spond to heterospecific calls. Further research on interspecific
eavesdropping could use synthetic calls to isolate the specific
acoustic properties that prompt responses to unfamiliar alarm
calls as well as investigating the learning mechanisms that allow
interspecific responses to dissimilar alarm calls.
FUNDING
Australian Research Council (Discovery Grant DP0665481 to
R.D.M.).
We thank Hwan-Jin Yoon for statistical advice and Tonya Haff,
Branislav Igic, Naomi Langmore, Justin Welbergen, and 2 anonymous
reviewers for valuable feedback on the manuscript. Michael and
Lesley Brooker, Alan Burbidge, Perry and Alma deRebeira and
Eleanor Russell provided accommodation and advice on field sites,
and Michael and Sandy Clinch at Nallan Station allowed us to record
on their property. Thanks to those who assisted us with recording calls
in the field: Demetrios Bertzeletos, Caroline Blackmore, Helen
Gardner, Peter Marsack, and Cathy O’Reilly. This study was carried
out with approval from the Australian National University Ethics Com-
mittee and under permits from the Australian Bird and Bat Banding
Scheme, the Australian National Botanic Gardens, the Department of
Fallow et al. • Acoustic similarity provokes responses to alarm calls
Environment and Conservation (Western Australia; SFOO5652 and
CE001538), Environment ACT (Australian Capital Territory), and
the New South Wales Department of Environment and Conservation
(S11897).
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