Behavioral Ecology
doi:10.1093/beheco/arq155
Advance Access publication 12 October 2010
Danger may enhance communication: predator
calls alert females to male displays
Emma I. Greig and Stephen Pruett-Jones
Department of Ecology and Evolution, University of Chicago, 1101 East 57th St., Chicago, IL 60637,
USA
Sexual displays are typically given in the absence of predators. One possible exception to this is seen in male splendid fairy-wrens
(Malurus splendens), which sing display-like vocalizations (Type II song) in response to predator calls. In this study, we explored
the function of this vocal ‘‘hitchhiking’’ using playback experiments. We documented that: 1) males responded to Type II songs
of other males as if they were displays intended for conspecifics, 2) females became more attentive after hearing a predator
vocalization than a control (nonpredator) vocalization, and 3) females tended to respond more strongly to Type II songs when
the songs were preceded by a predator vocalization than when they were given solo. Males of all age and status classes produced
Type II songs and production was not dependent on any of 3 morphological measures of male quality, so we do not find evidence
to support the hypothesis that Type II singing behavior is condition dependent. Because predator calls increased female
attentiveness and tended to increase subsequent response to Type II songs, it appears that males may be using predator vocalizations as alerting signals for their own conspecific-directed displays. Key words: acoustic displays, alerting signals, Malurus
splendens, predator calls, sexual selection, signal detection. [Behav Ecol 21:1360–1366 (2010)]
nderstanding the evolution of elaborate sexual displays
requires study of the signals themselves and the context
in which the signals are given. One context that is counterintuitive is displaying in the presence of predators, and with few
exceptions (e.g., Evans et al. 2002; Ellis 2009; Kim et al. 2009)
most research to date has demonstrated that both signalers
and receivers should reduce sexual behavior when predators
are near (Magurran and Seghers 1990; Magnhagen 1991; Zuk
and Kolluru 1998; Godin and McDonough 2003; Bernal et al.
2007; Møller et al. 2008). Displaying to conspecifics in the
presence of a predator, however, could be an adaptive strategy
under honest signaling theory (Zahavi 1975) if high-quality
individuals perform such potentially costly displays more than
low-quality individuals (Møller et al. 2006). Alternatively, displaying in the presence of predators could be advantageous
based on theories of efficient signal detection (Johnstone
1998; Rowe and Skelhorn 2004; Wiley 2006) because receivers
may be especially attentive when danger is near (Elgar 1989).
Thus, the presence of a predator may stimulate male sexual
displays if alerted or ‘‘scared’’ females are more receptive to
conspecific signals.
Although displaying to conspecifics in the presence of predators is considered to be the exception rather than the rule,
3 species of fairy-wrens (Aves: Maluridae) exhibit a vocal behavior that involves ‘‘hitchhiking’’ their song to the end of heterospecific vocalizations, specifically those of avian predators
(Langmore and Mulder 1992; Zelano et al. 2001; Greig et al.
2010). Our study focused on the splendid fairy-wren (Malurus
splendens) in which males give trills, ‘‘Type II songs,’’ in response
to the vocalizations of gray butcherbirds (Cracticus torquatus)
(Zelano et al. 2001; Greig and Pruett-Jones 2008). Butcherbirds
are potential predators of both adult fairy-wrens and their nests
(Lea and Gray 1935–1936; Tarburton 1991; Gardner 1998).
U
Address correspondence to E.I. Greig. E-mail: blufinch@uchicago
.edu.
Received 23 January 2010; revised 31 August 2010; accepted 5
September 2010.
The Author 2010. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
Nevertheless, butcherbird vocalizations cause male fairy-wrens
to sing so promptly and reliably that the joint vocalizations
resemble a duet (Greig and Pruett-Jones 2009). Working with
superb fairy-wrens, which also give Type II songs in response to
avian predator calls, Langmore and Mulder (1992) hypothesized that Type II songs are sexual displays directed to females
and that predator calls function as alerting signals that increase
signal efficacy. They also suggested that giving a display in response to an unpredictable external stimulus adds a dimension
of difficulty that enforces the honesty of the signal.
Two alternative reasons to sing in response to a predator are
to give an alarm directed to conspecifics or as a pursuit deterrent directed to the predator. We can reject these possibilities
in splendid fairy-wrens, however, based on previous results
(Greig and Pruett-Jones 2009) that strongly suggest that neither is the case. In particular, males do not give Type II songs
in the presence of silent butcherbirds but only in response to
butcherbird vocalizations. Additionally, in response to butcherbird playbacks, males are no more likely to give Type II
songs in the presence of a butcherbird mount than in the
presence of a nonpredator mount (Greig and Pruett-Jones
2009). This leaves the possibility that Type II songs are a form
of sexual or territorial display to conspecifics.
Here, we experimentally tested the hypotheses that Type II
songs are displays directed to conspecifics and that predator
calls function as alerting signals for intraspecific communication. We predicted: 1) If Type II songs are displays to conspecifics, then males should respond to Type II songs from an
intruding male on their territory in an aggressive or territorial
manner, 2) if the purpose of giving Type II songs after a predator is to enhance signal detection, then females should become more alert and attentive after hearing the calls of that
predator, 3) if predator calls effectively enhance Type II song
detection, then females should be more responsive to Type II
songs when they are preceded by a predator vocalization. We
investigate the possibility that Type II singing is a conditiondependent signal of male quality, and we document additional conspecific-directed display behaviors given by male
fairy-wrens in response to predator vocalizations.
Greig and Pruett-Jones
•
Predators alert females to male song
MATERIALS AND METHODS
Study species
We worked on a color-banded study group of splendid fairywrens that has been monitored from 1992–1999 and 2004–
2009 (Pruett-Jones et al. 2010). Splendid fairy-wrens are a
cooperatively breeding, socially monogamous, and reproductively promiscuous passerine widely distributed throughout
southern and southwestern Australia (Rowley and Russell
1997; Webster et al. 2004). Both male and female splendid
fairy-wrens produce a song that is used in territorial encounters and during the dawn chorus, referred to as ‘‘Type I song’’
(Rowley and Russell 1997). Both primary and helper males,
but rarely females, also give Type II songs (Greig and PruettJones 2008). In addition to the predator context, Type II
songs are also given during the dawn chorus and occasionally
during the day in the absence of predators (Greig and PruettJones 2008). Both sexes also give ‘‘seet’’ alarm calls, short
trilled contact calls, and brief ‘‘chatter’’ calls that function
either as contact calls or mobbing calls depending on the
speed with which concurrent chatters are delivered (Greig
and Pruett-Jones 2008).
Playback experiments
Our playback experiments were conducted primarily during
the October–December breeding season of 2008 at the Brookfield Conservation Park (BCP) in South Australia. We included playback experiments conducted in 2006 and 2007
for an analysis of the condition dependence of male Type II
singing behavior. We recorded all vocalizations used in the
playback experiments at BCP using a Marantz PMD 660
solid-state digital recorder (D&M Professional, Itasca, IL),
44.1 kHz sampling rate, and a Sennheiser ME66 shotgun microphone capsule and K6 power module (Sennheiser Electronic Corporation, Old Lyme, CT). We checked the quality
of all recordings and filtered noise below 1.0 kHz using Raven
1.2 (Cornell Laboratory of Ornithology, Ithaca, NY). Playbacks were uncompressed Audio Interchange File Format
audio files. In the field, we used a Saul Mineroff Electronics
amplified field speaker (Saul Mineroff Electronics Inc.,
Elmont, NY) and an iPod mini (Apple Inc., Cupertino, CA).
We standardized the relative amplitude of playbacks in Raven
1.2 and then tested actual amplitude with the field playback
equipment using a Radio Shack sound–pressure level (SPL)
meter (model number 33–2050, Radio Shack Corporation,
Fort Worth, TX), set at C-weighting, fast response. Amplitude
was approximately 87.0 dB SPL (re 20 lPa) at 1.0 m for Type I
songs and Type II songs, 83.0 dB SPL for nondisplay controls,
and 90.0 dB SPL for butcherbird and nonpredator vocalizations.
We tested focal birds with vocalizations recorded from nonneighboring individuals (potential territory intruders), and
we used a different sample individual for every focal bird
and test vocalization within each experimental treatment
(playback type). We tested only birds that did not have young,
so all birds were at a similar nesting stage and generally responsive to playbacks. We conducted playbacks in the morning (0600–1100 h) while focal birds were on their territory
with their social mate and clearly visible. For each playback,
we positioned the speaker ;20 m from the focal bird at
a height ;1 m above ground.
We randomized the order of experimental treatments for
those individuals that received multiple treatments over the
course of a season. Focal birds received a maximum of one playback in a day, and when multiple playbacks were conducted on
an individual they were done within a period of no longer than
2 weeks. We observed focal birds for a minimum of 5 min
1361
before beginning the playback to be sure that there were no
disturbances, such as an intrusion from an extragroup fairywren or the appearance of a predator. In the event of a disturbance, we discontinued the trial and attempted it at another
time. We recorded the entire playback session using a Marantz
PMD 660 digital recorder so that we could accurately record
both fairy-wren vocal responses and dictated behavioral responses. Blind scoring of behavioral responses was not feasible
because we could not capture playbacks on video for subsequent analysis, so to compensate for this, we chose behavioral
responses that were unmistakable when the bird was in view
(described below) and that happened immediately after or
during the playback. Because the behavioral responses we
chose were typically immediate and brief, we were not able to
dictate information on latency and duration that was accurate
enough for analysis, so we categorized these responses simply as
present/absent. Although this results in a more simplified data
set, the data are less susceptible to interpreter bias and error. If
a focal bird moved out of view and prevented unambiguous
scoring of a response, then we excluded the playback from our
analysis of that response. We still used that playback for analysis
of other responses that we were able to score unambiguously.
Because vocal responses were captured on a digital recorder
and their presence or absence confirmed subsequent to
the playbacks, these response variables were not subject to
interpreter bias.
To determine male response to Type II songs, we used 3
playback types: 1) a display (Type I) song (n ¼ 15), 2) a Type
II song (n ¼ 16), or 3) a nondisplay control that was a series of
3–4 seet alarms (n ¼ 9), contact calls (n ¼ 11), or chatter calls
(n ¼ 5). Spectrograms of all vocalization types are shown in
Greig and Pruett-Jones (2008). We recorded 3 nonexclusive
responses: ‘‘look,’’ ‘‘sing’’ (Type I song), and ‘‘chase female.’’
We chose the response variable ‘‘look’’ to capture changes in
vigilance to different playback types. A look response
consisted of a male turning his body or changing perches to
face the speaker. We chose the response variable ‘‘sing’’
because Type I songs are regularly given by males during
territorial encounters (Payne et al. 1988; Rowley and
Russell 1997; Greig and Pruett-Jones 2008) and therefore
likely represent an aggressive response to a conspecific in
this context. Using Raven 1.2, we created spectrograms of
the playback trial and measured the latency of song responses
as the time from the end of the playback to the beginning of
the song response. We considered songs that overlapped the
playback as having a latency of zero. We chose the response
variable ‘‘chase female’’ because it was an unambiguous response that occurred immediately after the playback and consisted of the male flying directly to his social mate and
displacing her multiple times in quick succession. Although
we were unsure if the chase response functioned in mate
guarding or display, it undoubtedly indicated a heightened
state of agitation during a territorial intruder. Focal birds
would often move into vegetation and out of view during
chase responses, so we were not able to determine precise
duration information and so code chases simply as present
or absent.
Because our playbacks consisted of only a single song or brief
series of nondisplay calls, males did not engage in prolonged
territorial responses of the sort typically observed in playback
studies, such as flying toward the speaker or singing multiple
response songs. These prolonged territorial responses can be
readily elicited from splendid fairy-wrens using playbacks of
multiple songs (Payne et al. 1988; Greig EI and Pruett-Jones S,
personal observation), but we wanted to keep our playback
regime as simple as possible and therefore chose to only use
playbacks of single songs and measures of immediate or nearimmediate responses.
Behavioral Ecology
1362
To determine female response to predator and nonpredator
calls, we used 2 playback types: 1) a butcherbird (n ¼ 18), or
2) a nonpredator (n ¼ 18). For the nonpredator category, we
used vocalizations of 3 species that were common in the park,
do not prey on adult fairy-wrens (Slater et al. 1989), and that
frequently produced loud conspicuous vocalizations: whitewinged choughs (Corcorax melanorhamphos), galahs (Cacatua
roseicapilla), and gray shrike-thrushes (Colluricincla harmonica).
We recorded 3 nonexclusive response variables: ‘‘look,’’ ‘‘fly,’’
and ‘‘seet’’ (alarm call). We conducted all of these playbacks
when females were on the ground foraging, so the ‘‘look’’
response always consisted of the female ceasing her foraging
behavior and standing erect while looking toward the speaker.
The ‘‘fly’’ response consisted of the female ceasing her foraging behavior and flying from the ground to nearby vegetation.
These behavioral responses either did not occur at all or occurred immediately after the playback such that variation in
latency was too small to accurately dictate into the microphone. We attempted to record details on the destination of
female flight (e.g., to covered or to open vegetation), but this
proved problematic because categorization of vegetation was
often ambiguous, and the initial location of females at the
time of playback determined what types of vegetation were
available and at what relative distances. Thus, we do not consider destination of flight variables further. ‘‘Seet’’ calls were
captured on the audio recordings so we were able to extract
accurate information on latency and number of calls, but
because seet calls were never given in response to nonpredator playbacks, coding seet response simply as present or absent sufficiently captured variation between playback types, so
we do not analyze seet responses in more detail.
To determine female response to solo and butcherbirdpreceded Type II songs, we used 3 playback types: 1) a solo
Type II song (n ¼ 25), 2) a solo butcherbird call (n ¼ 18), or
3) a Type II song preceded by a butcherbird call (n ¼ 20)
(Figure 1). We used the results from butcherbird playbacks
from the previously described playback series in this analysis
because those playbacks were conducted in the same manner
and during the same time frame. To create the butcherbirdpreceded Type II song playbacks, we used Raven 1.2 to join
a butcherbird recording and a Type II song, with a delay between vocalizations of 0.2–0.5 s. We used the same pool of
butcherbird calls and Type II songs as for the solo butcherbird
and Type II song playbacks; however, we were careful never to
test a female with the same butcherbird call or Type II song
she had heard before. We recorded the response variables
‘‘look’’, ‘‘fly’’, and ‘‘sing’’ (Type I song). We chose the response
variable ‘‘sing’’ because females will occasionally give Type I
songs in response to territorial intruders (Payne et al. 1988;
Rowley and Russell 1997; Greig and Pruett-Jones 2008). The
function of female song in response to intruding males may
be either territorial (e.g., Cooney and Cockburn 1995) or may
Figure 1
Spectrogram of a butcherbird
vocalization followed by a Type
II song that was constructed
and used for playback to females. BB indicates the beginning of the butcherbird call
and TII indicates the beginning of the Type II song.
be for the purposes of encouraging extrapair displays (e.g.,
Langmore 2000), but in either case it represents a response to
an intruding individual and therefore allows us to measure
the degree of female interest in a male playback. We chose
the response variables ‘‘look’’ and ‘‘fly’’ to capture changes in
female vigilance among playback types.
Condition dependence of Type II singing behavior
We collected 5 morphological and social indicators of male
condition: 1) age, either known or minimum age, 2) social
status, breeder or helper, 3) body condition, residuals of a regression of mass on tarsus length, 4) cloacal protuberance
volume (Tuttle et al. 1996), and 5) percent blue on breast,
range from 0% in completely brown males to 95% in very blue
individuals (Tarvin et al. 2005). Percent blue on breast was
estimated visually in the field and was done by the same observer (S.P-J.) for all males so that any error or subjectivity in
the estimation was consistent across males. To determine male
tendency to sing Type II songs, we played a single butcherbird
recording to each of 90 males and noted whether or not the
focal male gave a Type II song in response, which always occurred immediately after the playback or not at all. We used
31 different butcherbird recordings, and each male was tested
only once. For descriptive purposes, we also recorded the
occurrence of 3 display behaviors associated with butcherbird
playbacks; ‘‘face fan’’ (erecting and spreading the cheek
feathers; Rowley and Russell 1990) ‘‘sea horse flight’’ (slow,
upright, undulating flight; Rowley and Russell 1990), and
‘‘chase female.’’ We played 1–4 additional consecutive butcherbird recordings when documenting these display behaviors,
which often occurred after the second or third butcherbird
playback.
Statistical analysis
For playback experiments, we used 2-tailed Fisher’s Exact tests
to investigate pairwise comparisons of interest in response
variables. Because our comparisons were planned (a priori)
based on the experimental design and our questions of interest, we do not make Bonferroni adjustments to P values and
consider results significant at P 0.05.
For our analysis of the condition dependence of male Type II
singing behavior, we scored male Type II response as 1 (yes) or
0 (no) and used logistic regression for continuous variables
(body condition, cloacal protuberance volume, and % blue
on breast) because this test does not require normality in the
data. We used a chi-square distribution to test for an effect of
age on Type II singing behavior and categorized age as 1, 2, 3,
or 41. We used a Fisher’s Exact test to compare Type II song
responses of breeder and helper males. We did not conduct
additional multivariate analyses because testing each condition
Greig and Pruett-Jones
•
Predators alert females to male song
1363
Number of males with positive response
variable independently biases us toward detecting an effect, but
we found no effect for any variable and had a sufficiently large
sample size (n ¼ 90) to minimize Type II error.
RESULTS
Males were more likely to sing and tended to chase their mate
more in response to Type I (display) songs and Type II songs
than to nondisplay calls (Table 1; Figure 2), although the
difference in chase response between Type II songs and nondisplay calls was nonsignificant (P ¼ 0.052). There were no
significant differences in song latency or occurrence of male
sing or chase responses between Type 1 and Type II songs, and
there were no significant differences in male look responses
between any of the 3 playback types. Thus, only Type I and
Type II songs elicited behaviors consistent with territorial aggression or agitation, although males became more attentive
in response to all playback types.
Females were significantly more likely to look, fly, and seet
in response to butcherbird calls than in response to nonpredator controls (Table 2; Figure 3). Females were also more
likely to look and fly in response to butcherbird calls than in
response to solo Type II songs, more likely to fly in response to
butcherbird-preceded Type II songs than solo Type II songs,
and tended to look more in response to butcherbird-preceded
Type II songs than solo Type II songs (Table 3; Figure 4),
suggesting that butcherbird calls increased female attentiveness more effectively than Type II songs. This is supported by
the observation that, for the butcherbird-preceded Type II
song playbacks, the look and fly responses always occurred
immediately after the butcherbird vocalization and before
the Type II song had begun to play.
Females sang significantly more frequently in response to
butcherbird-preceded Type II songs than solo butcherbird calls
and tended to sing more often in response to butcherbirdpreceded Type II songs than solo Type II songs (Table 3;
Figure 4). The female song response always occurred after
the Type II song had played, so it was not in response to the
butcherbird call but rather in response to the Type II song
that followed the butcherbird call. Butcherbird-preceded Type
II song playbacks were longer (mean 6 standard deviation
[SD] ¼ 4.6 6 0.84 s) than either solo Type II (1.85 6 0.39 s)
or solo butcherbird (2.32 6 0.86 s) playbacks, but within the
butcherbird-preceded Type II song playbacks (range: 3.19–
7.06 s), variation in playback length had no effect on female
look, fly, or sing responses (logistic regression; look, v2 ¼ 0.69,
Table 1
Male response to Type I song (TI), Type II song (TII), and
nondisplay (ND) playbacks
TI (15)
TII (16)
ND (25)
Response
Yes
No
Yes
No
Yes
No
P
Look
Chase
8
3
6
12
9
3
6
13
17
0
5
25
Sing
6
8
5
8
0
25
Song
Latency
1.20 6 1.13 s
NS
0.046
0.052
0.001
0.003
NS
1.37 6 1.54 s
—
TI
TII
TI
TII
Sample sizes are given in parentheses after each playback type. Song
latency is given as mean 6 SD. P values are shown for comparisons of
either Type I (TI) or Type II (TII) verses nondisplay playbacks. No
significant differences exist between comparisons not shown. All tests
are 2-tailed Fisher’s Exact tests.
25
Look
Chase
Sing
20
15
10
5
0
TI
TII
ND
Figure 2
Number of males with positive (yes) responses for 3 response
variables look, chase, and sing recorded for 3 playback types. TI
represents display songs, TII represents Type II songs, and ND
represents nondisplay vocalizations (seet, contact, and chatter calls).
Error bars indicate binomial standard error.
n ¼ 19, P ¼ 0.404; fly, v2 , 0.01, n ¼ 20, P ¼ 0.980; sing, v2 ¼
0.26, n ¼ 20, P ¼ 0.606).
Males giving Type II songs in response to butcherbirds were
not significantly different than those not singing for all 5 social
and morphological traits (P . 0.40 for all comparisons).
When females (social mates) were present during the playbacks, males occasionally (in 15 of 78 cases, 19.2%) exhibited
additional display behavior, primarily face fans, in response to
butcherbird playbacks. Face fans were usually conspicuously
directed toward the resident female, which was evident because the focal male would move close to the female and face
her during the display.
DISCUSSION
The response of male fairy-wrens to both Type I and Type II
songs strongly suggests that Type II songs are displays directed
to conspecifics, despite often being associated with the presence of a predator. The degree to which Type II songs are territorial or sexual in nature is uncertain, but they are clearly
functionally distinct from nondisplay vocalizations such as
seet alarms and contact calls, which elicited no sing or chase
responses in males. It is noteworthy that nondisplay vocalizations elicited the same proportion of look responses as Type I
and Type II songs because it confirms that the lack of territorial response to these nondisplay vocalizations was not because males were unaware of the playback but instead
because males were not motivated to respond in a territorial
manner. The number of sing and chase responses to Type I
Table 2
Female responses to nonpredator (NP) and butcherbird (BB)
playbacks
NP (18)
BB (18)
Response
Yes
No
Yes
No
Look
Fly
Seet
8
3
0
10
14
18
15
13
11
1
5
7
P
0.003
0.002
,0.001
Sample sizes are given in parentheses after each playback type. All
tests are 2-tailed Fisher’s Exact tests.
Behavioral Ecology
20
Number of females with positive response
Number of females with positive response
1364
Look
Fly
Seet
18
16
14
12
10
8
6
4
2
0
BB
Table 3
Female responses to butcherbird (BB), Type II song (TII), and
butcherbird-preceded Type II song (BB 1 TII) playbacks
TII (25) BB 1
TII (20)
Response Yes No Yes No Yes No P
15
1
6
11
13
6
Fly
13
5
4
15
12
7
1
17
2
23
7
13
Sing
0.001
0.093
0.003
0.020
0.045
0.057
14
Look
Fly
Sing
12
10
8
6
4
2
0
TII versus BB
TII versus BB 1
TII versus BB
TII versus BB 1
BB 1 TII versus
BB 1 TII versus
BB
BB+TII
Figure 4
Number of females with positive (yes) responses for 3 variables look,
fly, and sing recorded for 3 playback types. TII represents a solo Type
II song, BB represents a solo butcherbird call, and BB 1 TII
represents a butcherbird vocalization immediately followed by a Type
II song. Error bars indicate binomial standard error.
and Type II song playbacks may appear low for a territorial
response (,50% of focal males responded), but it is important to note that these are responses to only a single intruder
song. The majority of males will sing and approach a speaker
in response to playbacks of multiple intruder songs (Payne
et al. 1988; Greig EI and Pruett-Jones S, personal observation),
so the comparatively low level of response is likely because our
intruder playbacks were brief. Thus, the sing responses from
focal males are likely to be territorial in function but simply
of a lower intensity than territorial responses to multiple
intruder songs.
In support of the interpretation that Type II songs are displays
directed toward conspecifics is the observation that butcherbird
playbacks sometimes caused focal males to engage in visual
display behaviors such as face fans and sea horse flights, which
were directed toward females and were often paired with Type
II songs. Not only were Type II songs sometimes used in conjunction with visual conspecific-directed displays but the fact
that butcherbird calls stimulated such visual displays supports
the idea that male fairy-wrens engage in courtship behavior in
response to predator vocalizations.
Our playbacks of butcherbirds and nonpredators to females
indicate that females can distinguish between predators and
nonpredators based solely on their vocalizations and that
butcherbird calls increase female vigilance more effectively
Look
16
TII
NP
Figure 3
Number of females with positive (yes) responses for 3 response
variables look, fly, and seet recorded for 2 playback types. BB
represents butcherbird playbacks and NP represents nonpredator
controls. Error bars indicate binomial standard error.
BB (18)
18
TII
TII
BB
TII
Sample sizes are given in parentheses after each playback type. P
values are shown for comparisons of interest. No significant
differences exist between comparisons not shown. All tests are 2-tailed
Fisher’s Exact tests.
than nonpredator calls. This may explain why males preferentially sing in response to butcherbirds rather than other avian
species (Zelano et al. 2001), if singing Type II songs after
heterospecific calls is a strategy for enhancing conspecific signal detection. Additionally, females tended to sing more in
response to butcherbird-preceded Type II songs than to solo
Type II songs, which is consistent with the interpretation that
hitchhiking a Type II song to a butcherbird call is an effective
communication strategy. One caveat of this result is that
butcherbird-preceded Type II song playbacks were longer in
duration than solo Type II song or solo butcherbird playbacks.
It is therefore possible that the increased level of female response to butcherbird-preceded Type II song playbacks was
due to the longer duration of that playback type rather than
the alerting properties of butcherbird vocalizations. Although
we cannot rule out that possibility using our current data
set, variation in playback duration within the butcherbirdpreceded Type II song playback type did not influence female
response, which suggests that playback duration may be less
important than playback content.
The function of female song in response to male Type II
songs remains uncertain. Females may be responding to intruding males in a territorial manner or may be singing in
response to Type II songs from intruding males because those
males represent potential extrapair partners. We did not consistently measure the responses of mates during playbacks to
focal birds and we therefore do not statistically analyze mate
response, but it is worth noting that after approximately 70%
of both solo butcherbird and butcherbird-preceded Type II
song playbacks, the female’s mate responded to the butcherbird vocalization with a Type II song. Because females did not
sing in response to solo butcherbird playbacks even when
their mate gave a Type II song, female song response appears
to be preferentially stimulated by butcherbird-preceded Type
II songs from intruding males rather than Type II songs from
their mate. Females were occasionally observed singing in response to Type I song and Type II song playbacks directed to
focal males, and in all cases, these were playbacks in which the
focal male sang a Type I song in response to the playback. In
the few instances where focal females sang in response to Type
II song playbacks directed to those females, these were also
accompanied by Type I song responses from their mate. Thus,
female song response seemed to be associated with mate Type
I song response, with the exception of female song response
Greig and Pruett-Jones
•
Predators alert females to male song
to butcherbird-preceded Type II songs; in these playbacks,
females sang even when their mate did not sing a Type I song.
Future work specifically investigating the influence of mate
response on focal female response would be valuable in determining the relative importance of territoriality and extrapair mate attraction in the function of female song, particularly
in response to butcherbird-preceded Type II songs.
Predator vocalizations may provide a form of costly signal
elaboration, either because it is dangerous to sing in the presence of a predator (Møller et al. 2006) or because it is difficult
to respond to such an unpredictable stimulus (Langmore and
Mulder 1992). These hypotheses predict that giving a Type II
song is condition dependent, but in all social and morphological traits measured for this study, males that gave Type II
songs in response to butcherbirds were not significantly different than nonresponding males. This may be because variation in a male’s motivation to sing Type II songs is more
dependent on immediate circumstances than on individual
condition. It is also possible that a male’s tendency to respond
to butcherbird calls is not adequately captured with a single
playback trial and measuring male Type II song responses to
multiple butcherbird playbacks is necessary to reliably estimate
Type II singing tendency. Even if singing a Type II song in
response to a predator is not a costly, condition-dependent
behavior, it is still possible that aspects of Type II song acoustic
structure, such as trill length (e.g., Dalziell and Cockburn
2008) or trill rate, contain condition-dependent information
about male quality.
We do not rule out condition dependence of Type II singing
behavior with our current data set, but the lack of evidence for
condition dependence is consistent with the idea that singing after a butcherbirdis analerting strategy that any male, regardless of
quality, can employ. In this scenario, the predator call functions as
an ‘‘attractive modifier’’ (Gualla et al. 2008) that does not necessarily make more obvious any information contained in the
male’s signal but simply makes the message more likely to be
received. Under this interpretation, the reason that females tend
to sing more in response to butcherbird-preceded Type II songs
than to solo Type II songs is because females are particularly alert
or ‘‘excited’’ after hearing a butcherbird call and are thus more
likely to detect and respond to subsequent Type II songs. The
observation that males sing only in response to conspicuous
predator vocalizations, but not in response to silent predators
(Greig and Pruett-Jones 2009), strengthens this interpretation; it
is not merely the presence of a potentially unnoticed silent predator that is important but rather the presence of an obvious
predator that has attracted the attention of receivers. Using
attentiveness caused by the presence of a predator to enhance
signal detection is akin to an individual adding alerting components to its own signals. Alerting components are simple,
conspicuous, easily recognizable additions that get a receiver’s
attention and precede a more complex message (Richards
1981). Organisms as taxonomically widespread as mammals,
birds, amphibians, and reptiles are thought to incorporate
alerting components into their signals (e.g., Gerhardt 1976;
Richards 1981; Mitchell et al. 2006; Ord and Stamps 2008) but
the effectiveness and extent of this phenomena have been
relatively little studied (Wiley 2006).
If the only requirement for an effective alerting signal is that
it attracts the attention of receivers, then vocalizations from
many species of avian predators could potentially be used
for this purpose. Splendid fairy-wrens at our study site, however, have a strong preference for singing Type II songs in response to butcherbirds and only sporadically sing in response
to vocalizations of other avian predators (Zelano et al. 2001).
Butcherbirds are sit and wait predators that hunt by swooping
to the ground to capture prey (Greig EI and Pruett-Jones S,
personal observation), so they may present a predation threat
1365
to fairy-wrens that are foraging in the open and unaware of
their presence but not to fairy-wrens that are alerted and in
vegetation. This would explain why fairy-wrens become attentive and fly to vegetation in response to butcherbird vocalizations but then appear to be willing to engage in behaviors
such as songs and face fans. Preferentially singing in response
to butcherbirds may therefore be because butcherbirds are an
ideal species to use as an alerting signal for conspecific display; they give conspicuous and recognizable vocalizations,
they require immediate attention by potential prey, and they
may not be extremely dangerous once potential prey are
aware of their presence.
We attempted additional playbacks in 2009 to determine if
nonpredator vocalizations also increased female response to
Type II songs or if butcherbird calls were unique in this
respect. These playbacks, however, were uninformative because
during that season female song response to all playbacks was
particularly low (and the comparison thus uninformative). We
suspect that the overall lack of female response was due to
their advanced nesting stage at the time of the playback
experiments compared to the previous year. Although a comparison of female response to butcherbird-preceded Type II
songs and nonpredator-preceded Type II songs would be
a valuable experiment, the lack of this experiment does not
undermine our current interpretation for 2 reasons. First,
even if nonpredator calls resulted in increased female response to Type II songs relative to solo Type II songs, that
would simply imply that heterospecific vocalizations other
than butcherbird calls may function as alerting signals, which
is not unreasonable. Second, the observations that females are
more attentive in response to butcherbirds and that males
preferentially sing Type II songs in response to butcherbirds
(Zelano et al. 2001) indirectly support the interpretation that
butcherbird calls are used by males because they make particularly effective alerting signals.
Sexual or territorial displays are typically thought to be negatively associated with the presence of predators, but our
results indicate that Type II songs are displays directed to conspecifics despite being closely associated with the presence of
a predator. Our results also suggest that that the presence of
a predator may actually enhance signal detection in receivers.
Predator-associated behaviors are often thought to have some
defensive antipredator function, but we have shown that may
not always be the case. We suggest that this signaling strategy
may occur in other species (e.g., fairy gerygones, Gerygone
palpebrosa; Murphy 2002) and need not apply only to auditory
traits but could be used for any signal that is more readily
detected by alerted receivers.
FUNDING
National Science Foundation to S.P-J.; University of Chicago
Hinds Fund; American Ornithologists’ Union; Animal Behaviour Society; Frank M. Chapman Memorial Fund; Graduate
Assistance in Areas of National Need training fellowship to
E.G.
We thank John Bates, Jill Mateo, Trevor Price, and Tim Wootton for
comments on the manuscript. Carolyn Johnson, Elizabeth Scordato,
and Jill Mateo loaned equipment for fieldwork. Nick Brandley, Katherine
Spendel, Bryce Masuda, Alex Tuchman, Karan Odom, Ben Parker, Leah
Fisher, Emily Kay, Alex Smith, and Caroline Novak provided assistance in
the field. Approval for all behavioral manipulations was obtained from
the University of Chicago Animal Care and Use Committee (ACUP
permit number 71708) and the Government of South Australia Department of Environment and Heritage (Wildlife Ethics Committee approval
number 21/2006, Scientific Research Permit number C25249 and animal use license number 187).
1366
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