Behavioral Ecology
doi:10.1093/beheco/arp055
Advance Access publication 1 June 2009
An avian eavesdropping network: alarm signal
reliability and heterospecific response
Robert D. Magrath, Benjamin J. Pitcher, and Janet L. Gardner
Department of Botany and Zoology, School of Biology, Australian National University, Canberra 0200,
Australia
Alarm calls potentially provide information about predators to heterospecifics, but little is known about patterns of eavesdropping among species. Many cases of eavesdropping in birds and mammals involve social species in mixed-species groups, but this is
not always true and the reliability of information may also be critical. We used a playback experiment and observations of natural
alarm calling to test for understanding of aerial ‘‘hawk’’ alarms among 3 species of passerine and assess call reliability. Superb
fairy-wrens and white-browed scrubwrens are ecologically similar and can share mixed-species flocks, whereas New Holland
honeyeaters are ecologically distinct and do not flock with the other species. Fairy-wrens and scrubwrens fled to cover to each
other’s alarm calls, but they also both fled to honeyeater alarms. Honeyeaters fled to scrubwren but usually not fairy-wren alarms.
The pattern of heterospecific responses appears related to call reliability from each species’ perspective. Honeyeaters called only
to predators of all 3 species and so provided reliable information to all. From a honeyeater’s perspective, fairy-wrens were least
reliable, as they gave 52% of their calls to nonpredators, whereas scrubwrens gave only 18% to nonpredators. However, from
a scrubwren’s perspective, fairy-wrens were largely reliable because most calls to nonpredators were to red wattlebirds, which pose
a physical threat to fairy-wrens and scrubwrens but not honeyeaters. We conclude that there can be mutual responses to alarm
calls between ecologically distinct species, that responses can be symmetrical or asymmetrical between species, and that call
reliability appears to affect response. Key words: aerial alarm calls, eavesdropping, interspecific communication, New Holland
honeyeater, predation, signal reliability, superb fairy-wren, white-browed scrubwren. [Behav Ecol 20:745–752 (2009)]
any species of birds and mammals give alarm calls to warn
of danger, and in some cases individuals respond to
the alarm calls of other species in addition to their own. For
example, Diana and Campbell’s monkeys (Cercopithecus diana
and Cercopithecus campbelli) respond to playback of each
other’s alarm calls (Zuberbühler 2000, 2001), as do yellowbellied marmots (Marmota flaviventris) and golden-mantled
ground squirrels (Spermophilus lateralis; Shriner 1998). Among
birds, many species respond to the mobbing calls of blackcapped chickadees (Poecile atricapillus; Hurd 1996; Templeton
and Greene 2007), and yellow-casqued hornbills (Ceratogymna
elata) even respond to the mobbing calls of Diana monkeys
(Rainey et al. 2004). Most evidence of response to heterospecific alarm calls concern mobbing calls, to which others
approach, but some species also respond to the flee alarm
calls of other species, by fleeing to cover or freezing (Munn
1986; Ramakrishnan and Coss 2000a; Magrath et al. 2007).
Although heterospecific alarm calls potentially provide important information about danger, they present the challenge
of assessing reliability, which is the probability that a call indicates danger to the listener (Searcy and Nowicki 2005). The
reliability of a heterospecific’s call is affected by at least 3
processes, all of which are also important within species
(Seyfarth and Cheney 1986; Møller 1988; Ramakrishnan and
Coss 2000b; Blumstein et al. 2004; Searcy and Nowicki 2005).
1) ‘‘Relevance.’’ Reliability depends partly on whether that
species is vulnerable to similar predators (Seyfarth and
Cheney 1990; Rainey et al. 2004; Ridley et al. 2007). If 2 species do not share threats, then the alarm calls of the other are
M
Address correspondence to R.D. Magrath. E-mail: robert.magrath@
anu.edu.au. B.J. Pitcher is now at Graduate School of the Environment, Macquarie University, Sydney.
Received 18 December 2008; revised 13 March 2009; accepted 15
March 2009.
The Author 2009. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
irrelevant ‘‘false alarms’’ and a totally unreliable cue of danger, whereas if the 2 species are equally vulnerable to the same
suite of predators, then the other species’ alarm calls are
a potentially relevant and therefore reliable source of information. Between these extremes, species may differ in their
vulnerability to different threats, so that another species may
provide only partially reliable information about the presence
of danger. 2) ‘‘Discrimination.’’ Species can differ in the reliability with which they discriminate between stimuli that are
threatening and nonthreatening. For example, within mixedspecies flocks in Sri Lanka orange-billed babblers (Turdoides
rufescens) appear to give alarm calls to any fast-moving aerial
object, rather than discriminating between raptors and harmless objects, whereas greater ratchet-tailed drongos (Dicrurus
paradiseus) are much more discriminating and therefore reliable (Goodale and Kotagama 2005). 3) ‘‘Deception.’’ Some
species use alarm calls deceptively. For example, bluish-slate
antshrikes (Thamnomanes schistogynus; Munn 1986), fork-tailed
drongos (Dicrurus adsimilis; Ridley et al. 2007) and great tits
(Parus major; Møller 1988) can use alarm calls as a way of scattering individuals of other species to steal food. Overall, therefore, individuals should be selected to respond differently to
different heterospecific alarm calls, depending at least partly on
the reliability of information from the listener’s perspective.
The response of 2 species to each other’s alarm calls could be
symmetric if each species is equally reliable to the other, or
asymmetric if there is a difference in reliability, such as if 1 species is vulnerable to a subset of threats to the other. For example, a small species may be vulnerable to both small and large
predators, and give alarms to both, whereas a larger species
may be vulnerable only to large species and give alarms only
to them (Cheney and Seyfarth 1990). Therefore, from the
small species’ perspective, all alarms by the larger species
are reliable cues of danger, whereas from the larger species’
perspective, only some alarm calls by the smaller species are
indications of danger. Depending on the relative frequency of
Behavioral Ecology
746
small and large predators, the larger species may be selected
to ignore or respond to the other species’ alarms, whereas the
smaller species should always respond to the larger species’
alarm calls. Asymmetric interspecific responses have parallels
in a greater response of some juveniles to adult alarm calls
than vice versa, if juveniles are vulnerable to a greater range of
threats or are less reliable callers (Ramakrishnan and Coss
2000b; Hanson and Coss 2001).
In addition to the adaptive costs and benefits of responding
to heterospecific alarm calls of different reliability, there could
be constraints on learning to recognize unreliable or infrequently heard calls. First, it could be difficult to learn that
the unreliable alarm calls of another species are indeed alarm
calls. If a large proportion of alarm calls by another species is
given when there is no danger to the listener, it may be difficult
to learn to associate the call with danger, even if it would be
adaptive to do so. In general, associative learning is likely to
be faster if a novel stimulus is more predictably associated with
the unconditioned stimulus (Shettleworth 1998; Bouton 2007).
Second, it may be difficult to learn even reliable alarm calls of
heterospecifics that are heard infrequently or those with whom
an individual does not have a close association, because there
may be limited opportunities to associate a call with danger.
Consistent with this constraint, many reports of heterospecific
responses to alarm calls entail species that form mixed-species
groups or mutualistic associations, in which there is the opportunity to learn the other’s calls (Nuechterlein 1981; Rasa 1983;
Burger 1984; Sullivan 1984; Munn 1986; Bshary and Noë 1997;
Zuberbühler 2000; Goodale and Kotagama 2005). Furthermore, many species responding to heterospecific calls are
themselves social, which may predispose these species to use
acoustic signals of danger (Lea et al. 2008). In other cases,
recognition of heterospecific calls depends at least on regular
exposure to those calls, which presumably allows associative
learning (Hauser 1988; Ramakrishnan and Coss 2000a).
There may be greater constraints on learning to recognize flee
alarm calls than mobbing calls. Mobbing alarm calls are often
loud, locatable and given repeatedly, and incite others to approach and monitor or harass a predator that is not posing an
immediate threat (Klump and Shalter 1984; Bradbury and
Vehrencamp 1998). All of these characteristics should facilitate
associative learning, as there is ample opportunity to listen to
the calls while approaching and observing the threat, and little
danger in doing so. By contrast flee alarm calls, such as those
aerial (‘‘hawk’’) alarm calls given by small birds to birds of prey,
are fleeting and associated with transient but immediate danger
(Marler 1955; Bradbury and Vehrencamp 1998). These characteristics are likely to make it more difficult to associate the call
with danger.
We used a playback experiment to test responses to heterospecific aerial alarm calls among 3 Australian passerines and
natural observations to assess whether any differences in
responses could be related to call reliability. Superb fairy-wrens
(Malurus cyaneus) and white-browed scrubwrens (Sericornis
frontalis) are social species that are vulnerable to the same
threats and can join mixed-species flocks. New Holland honeyeaters (Phylidonyris novaehollandiae) are pair breeders that
are vulnerable to only a subset of threats and do not form
mixed-species flocks with the other species. Fairy-wrens and
scrubwrens respond to playback of each other’s aerial alarm
calls (Magrath et al. 2007), and fairy-wrens also respond to the
honeyeater’s calls (Magrath et al. 2009) but it was unknown if
scrubwrens respond to honeyeaters or whether honeyeaters
respond to either of the smaller species. Our aims were to
determine first if responses among species are related to signal reliability from each species perspective. Given that honeyeaters are vulnerable to a subset of threats, they may be
less responsive to the other species than scrubwrens and
fairy-wrens are to each other and to honeyeaters. Second, if
mixed-species associations and sociality promote interspecific
understanding, then scrubwrens and fairy-wrens may be more
responsive to each other’s calls than to honeyeaters, and honeyeaters may be unresponsive to the other 2 species.
METHODS
Study site and species
We studied superb fairy-wrens, white-browed scrubwrens, and
New Holland honeyeaters, from March 2006 to November
2007 in the Australian National Botanic Gardens and Commonwealth Park, beside Lake Burley Griffin, Canberra (3616#S,
14906#), Australia. All species are common residents and accustomed to people. The Botanic Gardens occupy a 40 ha site that
includes plantings of Australian plants, native woodland, and
small areas of lawn (Magrath 2001). Commonwealth Park includes native and exotic vegetation and lawn. All sites used in
the study included a mix of trees, bushes, and more open areas.
The Botanic Garden fairy-wrens and scrubwrens were individually color-banded but honeyeaters were unbanded, as were the 3
groups (1 of each species) in Commonwealth Park.
Fairy-wrens (9–10 g; Maluridae) and scrubwrens (12–14 g;
Acanthizidae) are small cooperatively breeding passerines
(Magrath et al. 2000; Higgins et al. 2001; Magrath 2001).
These 2 species feed primarily on insects on the ground, their
territories overlap during the breeding season (eggs laid primarily from August to January), and they can occur together
in mixed-species flocks in the nonbreeding season (Bell 1980;
Higgins and Peter 2002; personal observations). Fairy-wrens
and scrubwrens breed in groups consisting of either pairs or
a dominant pair with 1 or more subordinate males, which are
usually philopatric individuals that act as helpers (Higgins
et al. 2001; Higgins and Peter 2002). At the study site, mean
group sizes are about 2.9 for fairy-wrens (Higgins et al. 2001)
and 2.7 for scrubwrens (Magrath and Whittingham 1997).
New Holland honeyeaters (Meliphagidae) are larger (ca. 19 g),
pair-breeding residents that also nest from August to January
(Frith 1976). They eat nectar supplemented with arthropods
and feed on flowers anywhere from ground level to the tree
canopy (Higgins et al. 2001).
All 3 species commonly give aerial alarm calls consisting of a
series of similar elements that are rapidly repeated (Higgins et al.
2001; Magrath et al. 2007, 2009). Calls consisting of a single
element do not always prompt flight by conspecifics. Scrubwrens respond to playback of multi-element calls by scanning or
fleeing, whereas they rarely flee, and often do not even scan, to
single elements (Leavesley and Magrath 2005). Similarly, fairywrens flee to multi-element alarms, but often do not do so to
single elements (Fallow P., Magrath R.D, unpublished data),
and only multi-element calls appear to prompt escape in honeyeaters (Higgins et al. 2001). In all species, therefore, single
elements might act as alert signals rather than flee alarms.
Fairy-wrens (mean peak frequency 9.1 kHz) and scrubwrens
(7.1 kHz) have high-pitched elements with a mean amplitude
of about 58 dB at 6 m (Leavesley and Magrath 2005; Magrath
et al. 2007), whereas New Holland honeyeaters have lowpitched elements (4.0 kHz) given at a mean of about 70 dB at
6 m (Magrath et al. 2009). Fairy-wren and scrubwren elements
are similar in having rapid frequency modulation about a constant carrier frequency, whereas honeyeaters have elements
with a monotonic decline in frequency. Fairy-wrens, at least,
appear to have to learn to recognize scrubwren alarms, despite
the similarities in element structure and frequency between
these species (Magrath et al. 2009).
All sites have resident populations of raptors and large avian
omnivores (Taylor and Canberra Ornithologists Group 1992),
Magrath et al.
•
Reliability and response to heterospecific alarm calls
and both groups of predators can prompt aerial alarm calls
from all 3 species (Leavesley and Magrath 2005; personal
observations). Raptors include the collared sparrowhawk
(Accipiter cirrhocephalus, ca. 120–220 g), which preys on small
birds up to about 25 g (Marchant and Higgins 1993). The pied
currawong (Strepera graculina, 300–340 g) is a common omnivorous predator that is known to take eggs, nestlings, fledglings,
and adults of small–medium-sized birds including fairy-wrens,
scrubwrens, and honeyeaters (Higgins et al. 2006). Grey butcherbirds (Cracticus torquatus, 80–95 g) have become resident,
although uncommon, in the Botanic Gardens since 2007 (personal observations) and are active predators of small passerines
(Higgins et al. 2006). Some other large resident species are
potential predators that are known to take eggs and nestlings
but rarely take free-flying birds. These include laughing kookaburras (Dacelo novaeguineae, 310–360 g kingfishers), Australian
ravens (Corvus coronoides, 620–680 g), and in 1 location silver
gulls (Larus novaehollandiae, 260–340 g; Higgins and Davies
1996; Higgins 1999; Higgins et al. 2006).
Large, aggressive red wattlebirds (Anthochaera carunculata;
100–120 g), another species of honeyeater, chase many other
species (Higgins et al. 2001). Wattlebirds fly at and occasionally strike and knock over fairy-wrens and scrubwrens, and we
have witnessed a death in a similarly sized species (Cockburn
A., personal observation). Honeyeater species in general
chase conspecific and heterospecific honeyeaters in defense
of nectar (Higgins et al. 2001), but we have never witnessed
wattlebirds physically strike New Holland honeyeaters, nor
have we seen New Holland honeyeaters chase fairy-wrens or
scrubwrens. Other local bird species are probably not a threat
to any of the focal species. Overall, therefore, all 3 focal species are vulnerable to the same suite of raptors and large
omnivores, but only fairy-wrens and scrubwrens are physically
threatened by red wattlebirds.
Playback experiment
In preparation for playback experiments, we prompted aerial
alarm calls using a gliding model collared sparrowhawk or pied
currawong, and recorded calls from a distance of 4–7 m with
a Sennheiser ME66 or ME67 directional microphone onto
a Marantz PMD670 digital recorder, sampling wave files at
44.1 kHz (Magrath et al. 2007, 2009). Details on glider design
are provided in Magrath et al. (2007). In brief, life-sized models were made of polystyrene foam body and wings, with a balsa
wood tail, shaped and painted to resemble either a collared
sparrowhawk or pied currawong. The wings were cut using
airfoil templates, so models could glide up to 25 m when
thrown by hand. As far as we can tell, alarm calls prompted
by models are acoustically indistinguishable from those
prompted by real predators (Magrath et al. 2007), the type
of model does not affect the alarm call (Magrath et al. 2007),
and birds respond to playback of prompted calls in the same
way as playback of calls prompted by natural predators or by
the calls of real birds (Leavesley and Magrath 2005; Magrath
et al. 2007). During playback experiments (below), calls were
matched across species according to the type of model that
prompted the call to ensure that no undiscovered differences
affected the results. There were 7 sparrowhawk- and 5 currawong-provoked calls for each of the 3 focal species.
The playback experiment tested whether each species
responded to the alarm calls of each other and whether the
naturally higher amplitude of honeyeater calls itself prompted
flight independent of call structure. We used a matched design
and broadcast 5 treatments in random order to 12 groups of
each species: 1) honeyeater alarm at a mean natural amplitude
of 70 dB; 2) honeyeater alarm reduced to a mean fairy-wren
and scrubwren amplitude of 58 dB; 3) fairy-wren aerial alarm
747
Figure 1
Spectrograms of sounds broadcast to birds. (a) Superb fairy-wren
alarm call; (b) white-browed scrubwren alarm call; (c) New Holland
honeyeater alarm call; and (d) crimson rosella contact bell call, as
a neutral control. Each focal group of a given species received unique
exemplars of playbacks sounds. Spectrograms were prepared in
Raven 1.3 with a Blackman window function, 2.27-ms time grid and
21.5-Hz frequency grid. Note the lower frequency scale for
honeyeater and rosella.
at 58 dB; 4) scrubwren alarm at 58 dB; and 5) the bell contact
call of a crimson rosella, a harmless parrot, as a control, at 70
dB (Figure 1). All amplitudes were measured outside at 6 m
from the speaker. The lower amplitude of 58 dB was chosen
because it falls between and within 2 dB of the recorded mean
amplitude of fairy-wren and scrubwren alarm elements recorded at that distance (Magrath et al. 2007). The reducedamplitude honeyeater call tested whether others recognized
these calls even when there was no cue from amplitude. Each
playback consisted of a single, multi-element alarm call, composed by pasting a single element at natural intervals. We
chose recordings of elements where there was a high signalto-noise ratio, minimal reverberation and no prominent
overlapping sounds. Fairy-wren and scrubwren alarm calls
consisted of 4 elements, which lay within the natural range
of each species (Magrath et al. 2007), whereas honeyeater
calls consisted of 8 elements, again within their higher natural
range (Magrath et al. 2009). We used multi-element calls because these prompt flight by conspecifics (above), and so provide a clear test of eavesdropping by heterospecifics. We
balanced the playback design so that each species was sampled
equally over time and space. To do this, we based playbacks
around blocked ‘‘triplets’’ consisting of 1 group of each of the
3 species. Within each triplet, we randomized the order of
species, and groups in each triplet were in a similar location
and received playbacks before moving to the next. Each playback exemplar was unique for a given species, and the same
set of playbacks was used on each member of the triplet, to
ensure comparability of results among species. Playbacks were
carried out between 2 October and 9 November 2007, which
was during the breeding season of all 3 species when none was
in mixed-species flocks. In all, we carried out 180 playbacks to
36 groups of birds of the 3 species.
Behavioral Ecology
748
Playbacks were carried out when the focal (closest) bird was
feeding at least 0.5 m from protective cover and about 8 m from
the observer, who then scored the bird’s ranked response as 0)
none; 1) scan (stop and look 1 s); 2) scan then flee, but land
out of cover; 3) scan then flee to cover; or 4) flee to cover without scanning first. However, most of the variation in response
was due to whether birds fled to cover rather than not responding or scanning, so we also analyzed the dichotomous response
of flee to cover without scanning first (1) or any other response
(0), as well as detailing scan responses in the text. A bird
needed to be undisturbed for at least 5 min before the initial
and subsequent playbacks, with the count restarted after any
natural alarm calls or predator disturbance. Playback to
fairy-wrens and scrubwrens occurred when they were on the
ground, the primary site of foraging, whereas playbacks to honeyeaters occurred when they were feeding on nectar, their primary source of food, and on the outer branches of a plant. We
avoided playbacks when either of the 2 other species was within
sight of the focal bird, or any other bird was in sight and within
about 10 m of the focal bird. Social groups were treated as the
unit of analysis because typically either all or no individuals
present fled after a playback, and the focal bird was not necessarily the same for different playbacks to that group. Groups
were identified by color bands for scrubwrens and fairy-wrens
in the Botanic Gardens; otherwise groups were distinguished
by spatial separation. During the playback period, we followed
groups to assess territories, and we also ensured that previously
used neighboring groups were present when carrying out playbacks on a new focal group. Playback sounds were broadcast
using a Sony CD Walkman D-EJ751 connected via an amplifier
to a Response Dome speaker (1.5–20 kHz), with equipment
mounted around the observer’s waist. The birds were habituated to people, so standing at a distance 8–10 m did not have
any obvious affect on their behavior, and all groups received
a control treatment (above).
The experimental procedures appeared to cause only shortterm disturbance to the birds. Model predators caused birds to
flee for cover and call, but they resumed normal activities
within seconds or minutes, and after prompting calls, we
moved to another group. Alarm call playbacks often caused
birds to fly to cover, but they resumed foraging quickly, usually
within a minute. Any one social group of birds received only 4
alarm call playbacks and 1 control over the 5-week period of
playbacks, leading to only a minimal increase in the natural
rate of alarm calling (combining the 3 species, there were
about 8 alarm calls per hour; below).
observations of natural calling context. We believe that these
playbacks would have minimal impact on natural calling rate,
and no impact on the relative rates of calling to different
prompts. First, birds never called after alarm call playbacks.
Second, birds returned to normal activity very soon after alarm
playbacks and did not respond to control playback; even 10 s
after playback, 42% of birds remained or were already out of
cover. Third, each alarm playback lasted less than a second, so
a total experiment contained less than 3 s of alarm playback.
Finally, the total rate of alarm playback was at most 4 calls per
hour, which is still below the natural rate of 8 calls per hour. For
2 early triplets, focal observations of alarm call context were
attempted on a later date than the playback. In 1 of these cases,
the honeyeater group could not be located, so there was a total
of 11 triplets that were matched for time and space in the focal
observations of calling behavior. Surveys were completed between 9 October and 9 November 2007.
Statistical analyses
Analysis of the playback experiment used Cochran Q Tests to
examine the change in probability of fleeing to cover according to repeated-measures playbacks within a group (Siegel and
Castellan 1988; Sokal and Rohlf 1995). We used 3 a priori,
overlapping subsets for analysis: 1) comparison of all 5 treatments, to test if the birds responded to at least 1 alarm call
more than the control; 2) comparison among those 3 playbacks in which all alarm calls were at natural amplitude; and
3) comparison among those 3 playbacks in which all alarm
calls were matched in amplitude. Analysis of natural observations of call context was based on the 11 matched triplets
(above). We tested for differences in both the probability of
calling within the focal 1-h sample, using Cochran Q Tests,
and the number of calls produced per hour, using Friedman
tests, and considered the complete sample as well as calls to
different categories of prompt. We classified prompts as confirmed predators (sparrowhawks, currawongs, and butcherbirds), nonpredators (other species excluding kookaburras,
ravens, and gulls that are potential predators), and species
that are nonthreatening to fairy-wrens and scrubwrens (nonpredators excluding red wattlebirds that attack these species).
We carried out all analyses in SPSS 13.0 for Macintosh (SPSS
Inc., Chicago, IL), and all tests were 2-tailed.
RESULTS
Playback experiment
Natural observations of alarm call context
We carried out 1-h focal watches for each focal group, and
noted every multi-element aerial alarm call, and the probable
cause of the call. Only multiple-element calls were tallied, because unlike single element calls they are unambiguous flee
alarm calls leading conspecifics to flee for cover (above).
Groups were again the unit of measurement and analysis, because it was difficult to isolate the caller for every call and
because eavesdroppers would also hear groups calling. Birds
were followed and observed from a distance of 6–15 m. The
observation protocol was designed to ensure that each species
was sampled equally over time and space, so that differences in
calling should not be biased by differences in exposure to potential prompts. Focal group observations were carried out on
the same matched triplets as were used in the playback experiment, with each triplet consisting of 1 of each species in a similar location. In most cases, watches were started when we
arrived at a focal group for the playback experiment. In these
cases, playbacks were carried out if the criteria for playbacks
were met (above), so that playbacks could occur during the
Each species fled to cover after playback of the alarm calls of
conspecifics and at least 1 heterospecific, whereas no individual fled after the control playback (Figure 2; Cochran Q tests
over all 5 treatments: fairy-wren, Q ¼ 48.0, df ¼ 4, P , 0.001;
scrubwren, Q ¼ 30.0, df ¼ 4, P , 0.001; honeyeater, Q ¼ 25.9,
df ¼ 4, P , 0.001). For further analyses, we exclude the rosella
control, first considering alarm calls at natural amplitude
among which the honeyeater call was loudest, and then consider playbacks when all were broadcast at the same amplitude.
Fairy-wrens and scrubwrens were equally likely to flee to conspecific and heterospecific alarm calls at natural amplitude,
but honeyeaters were less likely to flee to fairy-wren alarm calls
than their own or scrubwren alarm calls (Figure 2; Cochran Q
tests across all 3 alarm calls: fairy-wren, Q ¼ 0.0, df ¼ 2, P ¼
1.0; scrubwren, Q ¼ 4.0, df ¼ 2, P ¼ 0.14; honeyeater, Q ¼
10.4, df ¼ 2, P ¼ 0.006; McNemar pairwise tests with 2-tailed
exact probability: honeyeater vs. fairy-wren, P ¼ 0.02; honeyeater vs. scrubwren, P ¼ 0.6). Scan responses were infrequent
in all species (Figure 2). One fairy-wren scanned to a rosella
Magrath et al.
•
Reliability and response to heterospecific alarm calls
749
even when they were reduced in amplitude by 12 dB to match
those of the other 2 species. Again fairy-wrens and scrubwrens
were equally likely to flee to cover to all alarm calls, whereas
honeyeaters tended to be least likely to flee to fairy-wren alarms
(Figure 2; Cochran Q tests across all 3 alarm calls; fairy-wren,
Q ¼ 0.0, df ¼ 2, P ¼ 1.0; scrubwren, Q ¼ 1.6, df ¼ 2, P ¼ 0.45;
honeyeater, Q ¼ 8.9, df ¼ 2, P ¼ 0.01; McNemar pairwise tests
with 2-tailed exact probability: honeyeater vs. fairy-wren, P ¼
0.06; honeyeater vs. scrubwren, P ¼ 1.0). Again, scan responses were infrequent in all species (Figure 2). In response
to the soft honeyeater alarm, 2 scrubwrens and 3 honeyeaters
scanned without flying. Overall, there appeared to be a slightly
reduced response to the honeyeater alarm when broadcast at
the reduced amplitude, but clearly the response to natural
honeyeater alarm calls was not merely due to their being louder than conspecific alarm calls.
Natural observations of alarm call context
Figure 2
Response of (a) fairy-wrens, (b) scrubwrens, and (c) honeyeaters to
playback of conspecific and heterospecific aerial alarm calls.
Response is categorized by the bird’s first response: flee to cover
without scanning first, scanning with or without fleeing afterward, or
no response; n ¼ 12 playbacks of each type to each species. Playback
types were FW ¼ fairy-wren alarm call at 58 dB; SW ¼ scrubwren
alarm call at 58 dB; NH ¼ New Holland alarm call the mean natural
amplitude of 70 dB; NHR ¼ New Holland alarm call at reduced
amplitude (58 dB); and CR ¼ crimson rosella contact bell call at 70
dB as a control. All amplitudes were measured outside at 6 m from
the speaker (text).
control; 1 scrubwren scanned to a honeyeater alarm, 3 scanned
then flew (1 to cover) to scrubwren alarms, and 1 scanned to
a fairy-wren alarm; 1 honeyeater scanned then flew to cover to
a honeyeater alarm, 3 scanned to a scrubwren alarm, and 1
scanned then flew to cover to a fairy-wren alarm. Overall,
fairy-wrens fled immediately to cover to all alarm calls at natural
amplitude, scrubwrens to most, but honeyeaters usually did not
respond to fairy-wren alarm calls.
The flee response to honeyeater calls was not simply due to
their high amplitude compared with fairy-wren and scrubwren
alarm calls. Birds still usually fled to honeyeater alarm calls
During the 11 h of 1-h focal watches on each species, we heard
a total of 56 fairy-wren, 30 scrubwren and 8 honeyeater multielement alarm calls (Table 1). Calls were given to 2 species of
known predator, 3 species of possible predator, and 5 nonpredators. Most calls to nonpredators, however, were given
to red wattlebirds, which are a threat to fairy-wrens and
scrubwrens. In addition, outside the 1-h focal period, we
heard alarm calls by all species to collared sparrowhawks,
and by fairy-wrens to a flock of yellow-tailed black cockatoos
(Calyptorhynchus funerrus, large but harmless parrots), flying
overhead.
We saw prompts for 98% of fairy-wren calls, 90% of scrubwren calls, and 50% of honeyeater calls (Table 1). Alarm calls for
which we saw no prompt may have been false alarms, but it
seems likely that they were to prompts that we did not see, as
these types of calls are given to birds in flight that may quickly
disappear from view. The lower proportion of alarms for
which we saw a prompt in honeyeaters could be because, unlike the other species, honeyeaters are often high in trees and
so have a more commanding view. In 1 case, a honeyeater
called from a tree while looking over a building. Given the
likelihood that we did not see some of the prompts to which
birds called, we analyzed minimum values for calls to particular categories of prompt. For example, the proportion of calls
to known predators was calculated from the number known to
be given to predators as a proportion of the total alarm calls.
The most consistent pattern was that fairy-wrens called more
to nonpredators than did the other species. Fairy-wrens gave at
least 1 call to nonpredators in almost all focal watches (9/11),
whereas honeyeaters never did so and scrubwrens did so in
only 2 of 11 watches (Table 2a). The species differed in the
overall probability of giving an alarm call (Q ¼ 7.7, df ¼ 2, P ¼
0.02), largely because fairy-wrens were more likely than the
other species to call to nonpredators (Q ¼ 14.9, df ¼ 2, P ¼
0.001). By contrast, the 3 species did not differ in the probability of giving at least 1 call to a predator within the hour
sample (Q ¼ 3.7, df ¼ 2, P ¼ 0.2). Analyses of the rates of
alarm calling per hour produced similar results to the probability of giving at least 1 call (Table 2b). Fairy-wrens gave the
greatest number of calls per hour (Friedman; v2 ¼ 9.1, df ¼ 2,
P ¼ 0.01), largely because they called at a higher rate to nonpredators than other species (v2 ¼ 13.9, P ¼ 0.001). However,
there was also a trend toward a difference in the rate of calling
to predators (v2 ¼ 4.8, P ¼ 0.09).
Although fairy-wrens often gave alarms to nonpredators, and
so were unreliable from a honeyeater’s perspective, most of
those calls were to wattlebirds, which pose a physical threat
to fairy-wrens and scrubwrens, and so their calls were largely
reliable from the perspective of conspecifics and scrubwrens
Behavioral Ecology
750
Table 1
Number of aerial alarm calls given by fairy-wrens, scrubwrens, and honeyeaters during 11 1-h focal watches, with prompt if detected
(n 5 11 focal groups of each species)
Prompt
Number of calls
Common name
Species name
Predator of small birds?
Fairy-wren
Scrubwren
Grey butcherbird
Pied currawong
Silver gull
Laughing kookaburra
Australian raven
Red wattlebird
Noisy friarbird
Australian magpie-lark
White-winged chough
Australian magpie
Unknown
Cracticus torquatus
Strepera graculina
Larus novae-hollandiae
Dacelo novaeguineae
Corvus coronoides
Anthochaera carunculata
Philemon corniculatus
Grallina cyanoleuca
Corcorax melanorhamphos
Gymnorhina tibicen
Yes
Yes
Possible
Possible
Possible
Noa
No
No
No
No
Unknown
5
20
1
0
3
18
3
2
0
3
1
1
20
0
1
0
4
0
0
1
0
3
0
4
0
0
0
0
0
0
0
0
4
6
44
1
1
3
22
3
2
1
3
8
56
98
30
90
8
50
94
91
Total
% Known
a
Table 2
Alarm calling to different types of prompt by fairy-wrens,
scrubwrens, and honeyeaters
Species
Prompt type
Fairy-wren
Scrubwren
Honeyeater
(a) Number of 1-h watches with at least 1 alarm call
10
7
4
Anya
10
7
3
Knownb
c
7
4
3
Predator
9
2
0
Nonpredatord
10
7
3
Threateninge
f
4
0
0
Nonthreatening
(b) Mean number of calls per hour (range in parentheses)
5.09 (0–14)
2.55 (0–18)
0.73
Anya
5.00 (0–14)
2.27 (0–15)
0.36
Knownb
2.27 (0–10)
1.82 (0–15)
0.36
Predatorc
d
2.36 (0–8)
0.36 (0–3)
0.00
Nonpredator
e
4.27 (0–10)
2.27 (0–15)
0.36
Threatening
0.73 (0–4)
0.00
0.00
Nonthreateningf
a
c
d
e
f
Total
Red wattlebirds are not predators but chase other birds and can physically strike fairy-wrens and scrubwrens.
(Tables 1 and 2). From a scrubwren’s perspective, fairy-wrens
gave false alarms to the remaining harmless nonpredators in
only 4 of 11 focal hours, although scrubwrens were slightly
more reliable because they gave no such calls (Cochran Q ¼
4.9, df ¼ 1, P ¼ 0.05). The pattern was the same when analyzing the number of calls given to these harmless species:
fairy-wrens gave few calls to nonpredators, but scrubwrens
were nonetheless slightly more reliable (Friedman; v2 ¼ 4.0,
df ¼ 1, P ¼ 0.05).
b
Honeyeater
A higher frequency of ‘‘false alarms’’ to nonpredators by
fairy-wrens could arise because they call more frequently regardless of the prompt or because a higher proportion of their
calls is to nonpredators. We therefore examined the proportion of calls that were false alarms from each species’ perspective. We calculated the proportion of ‘‘false alarms’’ for each
hour watch on each species and used matched analyses based
on the triplets of 3 species. From a honeyeater’s perspective,
calls to all nonpredators are false alarms, and fairy-wrens gave
a significantly greater proportion of alarm calls to nonpredators than did scrubwrens (52% vs. 18%; Wilcoxon Signed
Ranks Test: n ¼ 11, Z ¼ 2.37, P ¼ 0.02). From the perspective
of scrubwrens, both other species were largely reliable. Wattlebirds were a threat, so calls only to the remaining nonpredators were false alarms. Honeyeaters never gave such false
alarms, and only 15% of fairy-wren calls were false alarms,
although the difference was almost significant statistically
(Wilcoxon Signed Ranks Test: n ¼ 11, Z ¼ 1.83, P ¼ 0.07).
From a fairy-wren’s perspective, neither of the other species
gave false alarms.
DISCUSSION
(0–4)
(0–2)
(0–2)
(0–2)
(a) Number of 1-h focal watches in which the focal species gave at
least 1 aerial alarm call. (b) Mean number of calls given per hour by
focal species, with range in parentheses. N ¼ 11, 1-h-long watches on
each species.
Includes known and unknown prompts.
Includes calls where prompt seen.
Includes known predators listed in Table 1, but excludes ‘‘possible’’
predators.
Includes nonpredators listed in Table 1, but excludes possible
predators.
Includes species threatening to fairy-wrens and scrubwrens, so
includes predators, possible predators, and wattlebirds.
Includes species nonthreatening to fairy-wrens and scrubwrens, so
excludes predators, possible predators, and wattlebirds.
The ecologically similar and group-forming fairy-wrens and
scrubwrens responded by fleeing to each other’s aerial alarm
calls with equal probability as their own, consistent with an earlier experiment. They also fled to the aerial alarm calls of New
Holland honeyeaters, despite the fact that they do not form
mixed-species flocks with honeyeaters. Furthermore, all species fled to cover after low-amplitude honeyeater calls, showing
that the response was not merely due to the naturally high amplitude of honeyeater calls. Honeyeaters responded to scrubwren alarm calls as strongly as to their own alarm calls, but
usually did not respond to fairy-wren calls. The difference in
responsiveness among species appeared to be related to differences in the reliability with which each species’ call indicated
a threat to the listening species.
A strong mutual response to heterospecific aerial alarm calls
occurred regardless of whether individuals shared mixedspecies flocks, but responses could be either symmetrical or
asymmetrical. Although neither fairy-wrens nor scrubwrens
form mixed-species flocks with New Holland honeyeaters, both
fled to the aerial alarm calls of these honeyeaters. Honeyeaters
in general tend to have loud, relatively low-pitched aerial alarm
calls (Jurisevic and Sanderson 1994a, 1994b), so they are
Magrath et al.
Reliability and response to heterospecific alarm calls
751
probably conspicuous at long range to many other species,
and perhaps act as a ‘‘community sentinel species’’ (Taylor
and Paul 2006), much like sentinel species in mixed-species
flocks (e.g., Munn 1986; Goodale and Kotagama 2005; Ridley
et al. 2007). Nonetheless, we also found that New Holland
honeyeaters responded by fleeing to cover as frequently to
white-browed scrubwren aerial alarms as their own, so that
the response was symmetrical between these species. In contrast to their response to scrubwrens, honeyeaters were less
responsive to fairy-wren alarm calls than fairy-wrens were to
honeyeater alarms, so these species responded asymmetrically
to each other’s calls.
The breadth of eavesdropping among these Australian passerines is consistent with other studies showing eavesdropping
among social vertebrates that can form mixed-species groups,
yet also revealing eavesdropping on other species in the community. Eavesdropping among members of mixed-species groups
occurs in both birds (e.g., Munn 1986; Goodale and Kotagama
2005) and mammals (e.g., Bshary and Noë 1997; Zuberbühler
2000), and may be most common in species that are themselves
social (Lea et al. 2008). Nonetheless, other studies have revealed eavesdropping among species that do not have a close
association. For example, some mammals eavesdrop on other
mammals (Shriner 1998) or birds (Seyfarth and Cheney 1990;
Lea et al. 2008; Müller and Manser 2008; Schmidt et al. 2008),
and there is 1 report of a reptile eavesdropping on bird alarm
calls (Vitousek et al. 2007). Among birds, eavesdropping on
mobbing calls appears to be common (Hurd 1996; Templeton
and Greene 2007), and field observations suggest that birds
also eavesdrop on the flee alarm calls of other species (Taylor
and Paul 2006). Our results show experimentally that birds can
eavesdrop on the flee alarm calls of ecologically distinct species
that do not share mixed-species flocks.
The patterns of responsiveness to heterospecific alarm calls
appear to be related to signal reliability from each species’ perspective. From the perspective of fairy-wrens and scrubwrens,
all honeyeater alarm calls where we knew the prompt indicated
a predator, so flight to cover is an appropriate response and
each of these small species fled to playback of honeyeater calls
as frequently as to their own. Similarly, fairy-wrens and scrubwrens provided largely reliable information about threat to each
other, and both fled to the other’s alarm calls. In this case, each
species also gave calls to the physically aggressive wattlebirds
but rarely gave alarm calls to harmless species. From a honeyeater’s perspective, scrubwrens were more reliable than fairywrens, with only 18% of scrubwren calls compared with 52%
of fairy-wren calls given to nonpredators. This difference in
reliability might explain the reduced response of honeyeaters
to playback of fairy-wren compared with scrubwren alarms.
The patterns of calling and reliability within the 3 Australian
species have parallels with alarm calling in mixed-species flocks
in Sri Lanka. Within those flocks, both orange-billed babblers
(T. rufescens) and greater racket-tailed drongos (D. paradiseus)
called frequently, but babblers were less reliable as about 73%
of calls were given to nonpredators, compared with only 36% for
drongos (Goodale and Kotagama 2005). Patterns of response to
playback were variable, but no heterospecific in the flock
responded significantly to babbler alarms, whereas both babblers
and ashy-headed laughing thrushes (Garrulax cinereifrons)
responded to drongo alarms (Goodale and Kotagama 2008).
Again heterospecific responses seem to be affected by alarm call
reliability.
Although fairy-wren alarm calls were relatively unreliable
from the perspective of honeyeaters, it is still puzzling how
rarely honeyeaters took cover or even scanned after fairy-wren
alarms. This is because the cost of not responding to a ‘‘true’’
alarm call is likely to be much greater than responding unnecessarily to a ‘‘false’’ one, in which situation even quite unreli-
able calls can select for a response (Koops 2004; Searcy and
Nowicki 2005). Consistent with this reasoning, in some species, unreliable or deceptive alarm calls can provoke a response even when they are more frequent than reliable calls
(Munn 1986; Gyger et al. 1987; Møller 1988; Searcy and Nowicki 2005). Furthermore, less reliable calls can provoke increased scanning even if they do not provoke fleeing to
cover (Ramakrishnan and Coss 2000a; Blumstein et al. 2004).
We suggest 3, not mutually exclusive, explanations for the
reduced response of honeyeaters to fairy-wrens but suggest that
learning constraints are most consistent with the results. 1)
‘‘Not adaptive to respond?’’ From a honeyeater’s perspective,
fairy-wrens combined a high probability that a call would be
a false alarm with a high rate of alarm calling per hour (a mean
of 5.1 alarms per hour), so the cost of responding to every fairywren alarm could be substantive. They therefore may have
been selected, or learned, not to respond to fairy-wren alarms
because of the cost of fleeing to cover unnecessarily. However,
against this hypothesis, it is surprising that honeyeaters that did
not flee to cover usually showed no response at all, rather than
scanning (Figure 2). The cost of scanning to false alarms
would seem to be low, and the potential benefit of scanning
to ‘‘true’’ alarms high. 2) ‘‘Hearing constraints?’’ Honeyeaters
may have difficulty hearing fairy-wren calls because, at a peak
frequency of 9.1 kHz, they approach the upper limit of hearing of at least some species of birds (Dooling 2004), and have
a higher frequency than their own calls (4.0 kHz) and those of
scrubwrens (7.1 kHz). However, against this idea, 3/12 honeyeaters fled immediately to cover after fairy-wren calls and 1
fled after scanning first, so it is within the hearing range of at
least some individuals, and is unlikely to be completely inaudible to others. If the fairy-wren call is toward the upper limit
of the honeyeater hearing range, then it is surprising that no
other individuals scanned after a fairy-wren playback, as one
would expect some honeyeaters to detect but not recognize
the fairy-wren call and so scan to gather more information
(Dooling 2004). 3) ‘‘Constraints on learning?’’ The high probability of false alarms by fairy-wrens should make it harder to
learn to associate these calls with danger and so recognize
them as alarm calls. The lack of scanning is explicable if some
birds had not learned that they were alarm calls but difficult
to explain under the other 2 hypotheses.
In conclusion, our results suggest that there could be a complex ‘‘eavesdropping network’’ among species in bird communities, even among species that do not form close associations
such a mixed-species flocks. A remaining challenge is to assess
more broadly the ecological and taxonomic diversity of species
involved, and the roles that reliability and learning play in patterns of responsiveness among species.
•
FUNDING
The Australian Research Council grant to R.D.M.
We thank Andrew Cockburn, Anastasia Dalziell, Bort Edwards, Jim
Forge, Peter Marsack, Helen Osmond, and Bob Phillips for practical
help with field research and Anastasia Dalziell, Pam Fallow, Tonya Haff,
Will Cresswell, and 2 anonymous referees for comments on the manuscript. This work was carried out under permits from the Australian
National Botanic Gardens, Environment ACT, Australian Bird and Bat
Banding Scheme, and the Ethics Committee of the Australian National
University.
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