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The capacity to modify vocal syntax to changes in social context is an important component of vocal plasticity and complexity in adult vertebrates, especially in human speech. The ecological significance of this behaviour has been well established in some avian species but not in mammals where complex, multisyllabic vocalizations are rare. The Brazilian free-tailed bat, Tadarida brasiliensis, is a mammal that sings like a bird, producing hierarchically structured songs that vary in the order and number of phrases (i.e. syntax) from one rendition to the next while simultaneously following specific organizational rules. Here, we used playback experiments to examine the function of songs and tested whether song syntax is correlated with social context. Free-tailed bats responded rapidly and robustly to echolocation calls that mimicked a bat flying past the roost but did not respond to conspecific song playbacks. We compared songs that were directed at a passing bat with songs that were produced spontaneously and found that bats produced longer songs with different phrase content and order when singing spontaneously than when singing to bats approaching their roost. Thus, free-tailed bats quickly varied song composition to meet the specific demands of different social functions. These distinct singing behaviours are similar to those of some songbirds, suggesting that bats and birds have converged upon a similar set of production modes that may reflect common neural mechanisms and ecological factors.
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Social context evokes rapid changes in bat song syntax
Kirsten M. Bohn
*
, Grace C. Smarsh, Michael Smotherman
Department of Biology, Texas A&M University, College Station, TX, U.S.A.
article info
Article history:
Received 11 December 2012
Initial acceptance 7 January 2013
Final acceptance 29 March 2013
Available online 3 May 2013
MS. number: A12-00940R
Keywords:
bat
echolocation
song
syntax
Tadarida brasiliensis
The capacity to modify vocal syntax to changes in social context is an important component of vocal
plasticity and complexity in adult vertebrates, especially in human speech. The ecological signicance of
this behaviour has been well established in some avian species but not in mammals where complex,
multisyllabic vocalizations are rare. The Brazilian free-tailed bat, Tadarida brasiliensis, is a mammal that
sings like a bird, producing hierarchically structured songs that vary in the order and number of phrases
(i.e. syntax) from one rendition to the next while simultaneously following specic organizational rules.
Here, we used playback experiments to examine the function of songs and tested whether song syntax is
correlated with social context. Free-tailed bats responded rapidly and robustly to echolocation calls that
mimicked a bat ying past the roost but did not respond to conspecic song playbacks. We compared
songs that were directed at a passing bat with songs that were produced spontaneously and found that
bats produced longer songs with different phrase content and order when singing spontaneously than
when singing to bats approaching their roost. Thus, free-tailed bats quickly varied song composition to
meet the specic demands of different social functions. These distinct singing behaviours are similar to
those of some songbirds, suggesting that bats and birds have converged upon a similar set of production
modes that may reect common neural mechanisms and ecological factors.
Ó2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
An important milestone in the evolution of animal communi-
cation is the transition from monosyllabic to polysyllabic vocali-
zations (Maynard Smith & Szathmáry 1995). While the information
in monosyllabic vocalizations is limited to changes in the acoustic
features of a syllable (phonology), multiple syllables add an entirely
new dimension of potential exibility and information, namely
syntax, or the way in which elements are ordered and combined.
The use of learned, multisyllabic vocalizations with exible syntax
is most widely seen in birds (Kroodsma & Miller 1996). Songbirds
are especially well known for the widespread use of multisyllabic
songs associated with mating and territorial defence (Marler &
Slabbekoorn 2004;Catchpole & Slater 2008). Syntax in birdsong
is salient (Balaban 1988), and social context may play a large role in
song structure and note use (Catchpole & Slater 2008;Byers &
Kroodsma 2009).
In contrast, most mammals produce monosyllabic, xed signals
with much less exibility than birds (Hammerschmidt & Fischer
2008;Snowdon 2009; but see Arnold & Zuberbühler 2006;
Clarke et al. 2006;Ouattara et al. 2009). Although various examples
of singing have been documented in mammals (Payne & McVay
1971;Mitani & Marler 1989;Davidson & Wilkinson 2002;Behr &
von Helversen 2004;Holy & Guo 2005;Clarke et al. 2006;Bohn
et al. 2009), there is no evidence that mammals alter song
composition and structure in ways comparable to songbirds. This
key behavioural distinction has been attributed to the general
absence of a neural substrate supporting vocal plasticity in mam-
mals that is present in both songbirds and humans (Doupe & Kuhl
1999;Jarvis et al. 2005;Kao et al. 2005;Jürgens 2009).
Cetaceans and bats may be exceptional since both groups have
evolved a suite of neural adaptations to support laryngeal echolo-
cation. They are the only two groups of mammals that demonstrate
vocal learning (Boughman 1998;Janik 2000;Foote et al. 2006;
Knornschild et al. 2010), juvenile babbling (Knörnschild et al.
2006), regional dialects (Cerchio et al. 2001;Ouattara et al. 2009)
and cultural transmission of vocalizations (Deecke et al. 2000;
Garland et al. 2011). If these behaviours are indicative of a neural
substrate that supports vocal plasticity, it is likely that some ceta-
ceans and bats may also possess the capacity to rapidly vary vocal
syntax in response to social cues.
Brazilian free-tailed bats, Tadarida brasiliensis, produce songs that
are remarkably similar acoustically and behaviourally to birdsongs.
Free-tailed bat songs follow a hierarchical structure where three
types of phrases (chirps, trills and buzzes) are in turn composed of
four types of syllables (Chirp A, Chirp B, trill and buzz; Bohn et al.
2009;Fig. 1). Free-tailed bat songs are highly exible while
following a clear and consistent syntax. The number and order of
phrases dynamically vary from one rendition to the next, while
*Correspondence and present address: K. M. Bohn, School of Integrated Science
and Humanity, Florida International University, Miami, FL 33199, U.S.A.
E-mail address: kbohn@u.edu (K. M. Bohn).
Contents lists available at SciVerse ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
0003-3472/$38.00 Ó2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.anbehav.2013.04.002
Animal Behaviour 85 (2013) 1485e1491
simultaneously adhering to a specic set of rules (Bohn et al. 2009).
Although some song typesare preferred over others (Fig. 1), the
number of repeats of trill and buzz phrases vary within each song
type. Thus, a few element types (in this case phrases) can be com-
bined to form a potentially enormous set of unique signals. This
combinatorial syntax(Hailman & Ficken 1986) has been observed in
only a handful of avian species including chickadees (Hailman &
Ficken 1986;Hailman et al. 1987;Ficken et al. 1994) parrots
(Wright & Dahlin 2007) and hummingbirds (Rusch et al. 1996).
As in songbirds, free-tailed bat songs are produced exclusively
by males and singing is especially pronounced during the mating
season. During this time, males establish territories that they
aggressively defend against other males, but in which they allow
females to reside (Bohn et al. 2008). However, males also sing year
round and in all-male colonies, so songs may function in other
social contexts besides mating. This is remarkably similar to
chickadee calls, which have combinatorial syntax that varies with
social (Ficken et al. 1994) and environmental (Soard & Ritchison
2009) context. Free-tailed bats have a large vocal repertoire
(Bohn et al. 2008), roost in the millions and have all-male, all-fe-
male or mixed-sex colonies that uctuate across seasons. Thus, the
broad diversity of song types may reect behavioural responses to a
highly variable social environment.
Due to the cryptic nature of bats, as well as the short duration,
fast tempo, and ultrasonic frequencies of their songs, it has been
difcult to discern specic stimuli or behavioural contexts that
evoke singing. Since visual cues are generally unavailable to detect
conspecics from within roost sites, we hypothesized that bats use
auditory stimuli to assess social context and that songs may be
primarily used to advertise maleshidden locations to ying con-
specics. In this study we used playbacks of echolocation passes
and conspecic songs to determine whether they evoke singing
and to test whether bats vary their songs with social context.
METHODS
Playbacks
We conducted 10 playback experiments, each at a different
location at a natural roosting site located on the Texas A&M Uni-
versity campus (College Station, TX, U.S.A.). Atthis site, bats roost in
discrete locations in cracks that run between the concrete slabs of
the football stadium. We selected 10 roost sites that were outside of
the hearing range of each other and placed two speakers and a
microphone within 0.25 m of the crack. Each playback experiment
consisted of two types of playbacks, echolocation and song. In
addition, we conducted ve echolocation playbacks within a vi-
varium using captive T. brasiliensis, where one male singer was
present at a time (N¼5 males). The Texas A&M Animal Care and
Use Committee approved all procedures and animal husbandry for
this research (protocol number number 2007-254). Stimuli were
played from a laptop computer running Avisoft Recorder
Ó
through
a PCMCIA card (NI DAQCard-6062E) to a Pioneer ribbon tweeter
(ART-55D), via a Sony power amplier (STR-DE598).
0
Time (ms)
700
100
0
100
0
100
0
Frequency (kHz)
ABAB
Trill Buzz
ABAB
ABBA
Trill
Buzz
Trill
Chirp
Chirp Chirp
Chirp
(a)
(b)
(c)
Figure 1. Spectrograms of songs produced by male free-tailed bats. (a) A bat produces a chirp-trill-buzz song type in response to an echolocation playback (Supplementary Audio
S1). (b) The same bat produces a chirp-trill-chirp song type spontaneously in the roost (Supplementary Audio S2). (c) A different bat produces a chirp-buzz song type
(Supplementary Audio S3). Upper case letters refer to the rst four Chirp A and Chirp B syllables. Note that for the song in (b), the complete phrase sequence is chirp-trill-trill-chirp,
but when dening song types, sequential repetitions of phrases are omitted.
K. M. Bohn et al. / Animal Behaviour 85 (2013) 1485e1491148 6
To create echolocation stimuli, echolocation passes were
recorded from ve males, one at a time, that were free ying in a
623m ight-room lined with acoustic foam. The micro-
phone (Bruel & Kjær, type 4939, ¼ inch) was placed in the centre
of the room where echolocation passes were recorded as the bats
ew over the microphone, resulting in an amplitude pattern that
mimicked a wild bats approach during playbacks (Fig. 2).
Although the echolocation passes recorded from captive bats
differed somewhat from those of wild bats, they were produced in
similar highly cluttered environments (at the wild colony, ca. 2 m
of space in front of each roosting site is surrounded by cement).
Echolocation passes were digitized with a National Instruments
DAQmx card, NI PCI-6251 (300 kHz, 16-bit sample rate) and Avi-
soft software (v.2.97, Avisoft Bioacoustics, Berlin). Song stimuli
were obtained from previous recordings we had performed in
captive colonies where songs were produced spontaneously in the
roosts (Bohn et al. 2009;Fig. 2). Three songs with high signal-to-
noise ratios were selected from each of ve males. For echoloca-
tion passes and songs, intervals between syllables were replaced
by silence, and a small (0.5 ms) taper was added to the beginning
and end of each syllable using Signal 4.0 (Engineering Design,
Belmont, MA, U.S.A.). Files were then band-pass ltered between
5 kHz and 80 kHz and peak-to-peak amplitudes were normalized
to 1.5 V.
One bout of three echolocation passes and one bout of three
songs were created for each caller (N¼5 for echolocation, N¼5 for
song) using random intervals from recordings (between 3.5 and
9.5 s for echolocation and between 0.3 and 5 s for song; Fig. 2). Each
echolocation playback and each song playback consisted of alter-
nating 270 s of background noise with one bout from each of the
ve callers in random order. Echolocation bout durations ranged
from 15 to 19 s, while song bout durations ranged from 6 to 13 s.
The different durations for echolocation and song stimuli resulted
in each echolocation playback lasting about 24 min and each song
playback lasting about 21 min. For all analyses we corrected for this
by examining the number of responses per second. In the labora-
tory, only echolocation playbacks were conducted. In the eld, the
entire echolocation playback and the entire song playback were
conducted in alternating order at each site.
Responses
Vocalizations were recorded and digitized using an Avisoft
CM16 condenser microphone and Avisoft Ultrasoundgate
Ó
1.5
Amplitude (V)
1
0.5
0
–0.5
–1
–1.5
1.5
Amplitude (V)
Frequency (kHz)
1
0.5
0
–0.5
–1
–1.50 2 4 6 8 10 12 14 16 18 20
80
70
60
50
40
30
20
10
0
Frequency (kHz)
80
70
60
50
40
30
20
10
0
0 0.2 0.4 0.6 0.8 1 1.2
Time (s)
(b)
(c)
(d)
(e)
Bout 1 Bout 2 Bout 3 Bout 4 Bout 5
270 s 270 s 270 s 270 s 270 s 20 s
(a)
Figure 2. Examples of playbacks. (a) Diagram of an entire playback of echolocation passes or songs. Each bout is from a different individual. (b) A bout of echolocation passes from
one bat. (c) A bout of songs from one bat. (d) Spectrograms of the boxed portion of (a). (e) Spectrogram of the boxed portion of (b).
K. M. Bohn et al. / Animal Behaviour 85 (2013) 1485e1491 148 7
(300 kHz/16 bit). Recordings were divided into four contiguous
periods: (1) 20 s pre, immediately preceding stimuli, (2) echo or
song, beginning with and encompassing stimuli, (3) 20 s post,
immediately following stimuli and (4) 230 s control. For responses,
songs were identied from other vocalizations by their unique
alternating temporal pattern of Chirp A and Chirp B syllables (Fig.1;
also see Bohn et al. 2009). We visually inspected all recordings and
noted the duration and phrase sequence (each chirp, trill and buzz
phrase) of every song. Additionally, because sequences were so
variable, we also categorized songs into song typesby excluding
repeats of trills and buzz phrases (Fig. 1).
Analyses
We examined the number of song responses in two ways. First,
we pooled responses across all experiments for each stimulus type
and for each playback caller (N¼5 batsecholocation passes, N¼5
batssongs) and used a randomized block design ANOVA with
playback caller as a block, and period (control, pre, echo/song, post)
and stimulus type (echo or song) as factors. To verify whether our
ndings were consistent across experiments and not due to one
exaggerated experiment, we performed an ANOVA as above, but
instead of pooling all responses, we kept each experiment separate
as a block (N¼10 sites in the wild). Statistics were conducted
identically for the captive colony experiments except they lacked
the song/echo effect (only echo playbacks were performed) and
there were only ve experiments, each on a separate subject.
Using the experiments conducted at the natural colony, we
compared song structure during two distinct contexts: songs pro-
duced during an echolocation pass (see Results,Fig. 3) and songs
produced spontaneously in the roost during control and pre pe-
riods of all playbacks. For this analysis, we did not use post periods
because song production was slightly elevated and may have been
in response to stimuli. We also did not use responses to song
stimuli because there were almost no songs produced during these
periods. Although we were unaware what specically triggered
spontaneous songs, we knew it was not a passing bat since no bats
were ying during these experiments.
First, we used a chi-square contingency test to compare the
frequency of the four most common song types (phrase order with
buzz and trill repeats ignored) and complete phrase sequences
(including repeats) between echolocation playback periods (echo)
and control/pre periods (spontaneous). To test whether individuals
modied songs between contexts, we identied individuals using
their Chirp B syllables, which are highly stereotyped within
individuals but vary among individuals (Bohn et al. 2008). We
identied eight bats for which we had at least 10 songs and per-
formed a logistic regression using context as a factor and subject as
a block on the same song type and phrase order categories as the
chi-square contingency test. In addition, we identied 21 bats for
which we had at least ve songs in both contexts and used paired t
tests to compare the duration of songs, the frequency of songs with
buzzes and the frequency of songs with trills between the two
contexts. Finally, for bats that produced trills or buzzes in at least
ve songs in both contexts (N¼15 and 18, respectively), we used t
tests to determine whether the number of repeats varied between
contexts.
RESULTS
During 10 playback experiments, we recorded songs at a rate of
more than 100 songs/h, with a total of 699 songs from 39 different
males (equipment failed during one song playback). Although the
number of singing males varied between roost sites, the density of
singers at a given site did not affect individual singing rates
(regression of average number of songs per male versus number
of males in a site: F
1,9
¼0.14, P¼0.7). Bats responded to echolo-
cation passes but not to conspecic songs (ANOVA: song/echo:
F
1,3 1
¼20.6, P<0.0001; control/pre/stimulus/post: F
3,31
¼29.0,
P<0.0001; interaction: F
3,31
¼24.8, P<0.0001; Figs 3,4a). The
only signicant difference following Tukey tests (alpha ¼0.05) was
between echolocation periods and all others. These effects were
robust in that the same results were found when data were ana-
lysed relative to each experiment (song/echo: F
1,359
¼25.8,
P<0.0001; control/pre/stimulus/post: F
3,359
¼36.3, P<0.0001;
interaction: F
3,359
¼31.0, P<0.0001).
Responses to echolocation passes were both rapid and robust.
Out of 50 sets of echolocation passes (N¼5 different batspasses
per playback, N¼10 playbacks), bats responded 74% of the time
with a total of 215 songs. During the interval immediately pre-
ceding stimuli, we recorded songs only 6% of the time across
all experiments (three songs). Echolocation-provoked singing
occurred very rapidly with onset latencies ranging from 200 to
500 ms (Fig. 3). We also ran echolocation playbacks on isolated
males in our captive colony and found similar results: singing was
rapidly and robustly provoked via playbacks of echolocation passes
(F
3,12
¼16.05, P¼0.0002; mean SE number of songs/20 s: echo
stimulus ¼5.8 1.2; pre ¼0.13 0.08; post ¼0.93 0.46; con-
trol ¼0.14 0.07; analysed relative to subject: F
3,54
¼15.6,
P<0.0001; Fig. 3;Supplementary Video S1,Audio S4).
0
10
20
30
–1400
–1200
–1000
–800
–600
–400
–200
0
200
400
600
800
1000
1200
1400
Number of songs
Time from stimulus onset (ms)
(b)
0
10
20
30 (a)
Figure 3. Number of songs produced by bats at 100 ms intervals relative to the start of stimulus onset of (a) songs (N¼135 stimulus songs, N¼10 response songs) or (b)
echolocation passes (N¼135 stimulus echolocation passes, N¼92 response songs). In (b), grey bars represent wild batsresponses; black bars are superimposed and represent
captive batsresponses (N¼28 songs, N¼45 echolocation passes).
K. M. Bohn et al. / Animal Behaviour 85 (2013) 1485e1491148 8
For the natural colony experiments, we tested whether the
composition of songs produced during the stimulus periods of
echolocation playbacks differed from those produced spontane-
ously in the roost. First, we examined the distribution of phrase
sequences and song types. There were a total of 69 different phrase
sequences, of which 52% were the four most common sequences:
chirp, chirp-buzz, chirp-trill-buzz and chirp-trill-trill-buzz). We
found no correlation between phrase sequences and context using
the four most common sequences and pooling the remainder into
an othercategory (
c
2
4
¼7:0, N¼587 songs, P¼0.14). There was
also no difference between contexts for eight bats that produced
at least 10 songs in each context (logistic regression:
c
2
4
¼4:2,
P¼0.28). There were 26 song types (phrase sequences excluding
trill and buzz repetitions (Fig. 1,Table 1), of which 84% were the four
most common types: chirp-trill-buzz, chirp-buzz, chirp-trill and
chirp. Comparing the relative frequency of these song types and a
fth othercategory between echolocation and spontaneous con-
texts revealed that more songs during echolocation passes were
chirp-trill-buzz than expected (38% of 213 echolocation response
songs versus 28% of 385 spontaneous songs), whereas more
spontaneous songs were chirp-trill (13% versus 7%) or chirp (22%
versus 15%) than expected (
c
2
4
¼13:0, P¼0.01). There was no
signicant difference in the frequency of chirp-buzz song types
(24% and 21% for echo and spontaneous, respectively) or in the
frequency of othersongs (16% in both contexts). We used a logistic
regression on the same song types with bat as a block and context
as a factor for eight bats that had at least 10 songs in each context
and found similar results (
c
2
4
¼22:0, P¼0.0002; mean percentage
of song types during echo and spontaneous contexts: chirp: 16%
and 26%; chirp-trill: 3% and 18%; chirp-buzz: 27% and 15%; chirp-
trill-buzz: 40% and 27%; other: 18% and 13%).
Next, we examined four song parameters for individuals that
produced at least ve songs in the two contexts: duration, number
of phrases, whether or not songs contained buzzes and whether or
not songs contained trills. We found that songs produced during
echolocation stimuli were signicantly shorter but also more
frequently included buzz phrases than spontaneously produced
songs (paired ttests: duration: t
20
¼2.8, P¼0.01, Fig. 4b; buzz
phrase: t
20
¼2.7, P¼0.01, Fig. 4c). There was no difference between
songs produced in the two contexts with respect tothe frequency of
trills (t
20
¼0.64, P¼0.53) or number of phrases (t
20
¼0.20,
P¼0.84). Finally, we tested whether the number of phrase repeats
differed between contexts for those songs that contained buzzes or
trills. We found no difference between contexts for the number of
buzz repeats (t
17
¼0.81, P¼0.43) or trill repeats (t
14
¼1.7, P¼0.10).
DISCUSSION
Playbacks mimicking the echolocation call sequences of passing
bats rapidly triggered stimulus-specic singing. The rapid response
and tight temporal correlation between the echolocation pulse
stimuli and the onset of the batssinging leaves little doubt that the
evoked songs were directed to the perceived presence of a passing
bat. Although our experiments were conducted during the day,
when few bats normally y (except between roosts), we obtained
the same results in the laboratory and when bats were actually
ying (Video S1). Thus, we are condent that bat song is a robust
and natural response to approaching conspecics. Conspecic song,
however, did not evoke singing, even though the spectrotemporal
acoustic structure of some song syllables are very similar to
Table 1
Distribution of song types produced by Brazilian free-tailed bats at the wild colony
during playback experiments
Song type Nsongs Percentage
chirp-trill-buzz 243 34.8
chirp-buzz 148 21.2
chirp 134 19.2
chirp-trill 65 9.3
chirp-trill-chirp 27 3.9
chirp-trill-chirp-buzz 27 3.9
chirp-trill-chirp-trill-buzz 17 2.4
chirp-trill-chirp-trill 5 0.7
Other (N¼18 song types) 33 4.7
26 song types 699
0
200
400
600
800
1000
Echo Spontaneous
Duration (ms)
Context
(b)
0
0.2
0.4
0.6
0.9
Echo Spontaneous
% with buzz phrase
Context
(c)
0
1
2
3
4
5
6
Pre Stimulus Post Control
Echo
Song
Number of songs/20 s
Period
(a)
Figure 4. (a) Songs produced by bats before (pre), during (stimulus) and after (post)
playback of echolocation and song stimuli, and during the control period (control). (b)
Song duration and (c) percentage of songs with buzzes produced in response to
echolocation stimuli and produced spontaneously (control and pre periods of (a)).
K. M. Bohn et al. / Animal Behaviour 85 (2013) 1485e1491 148 9
echolocation pulses (Bohn et al. 2008). This indicates that the
overlying temporal pattern of acoustic stimuli inuenced the bats
responses.
The rapid responses of bats to the echolocation pulses of
approaching conspecics exemplify the use of echolocation signals
for social interactions. By eavesdropping on echolocation signals,
males can sing when they are certain a conspecic is in audible
range. Interestingly, echolocation calls of approaching conspecics
also trigger song in the greater sac-winged bat, Saccopteryx bili-
neata (Knörnschild et al. 2012). In this species, different songs are
used based on the gender of the approaching conspecic, indicating
that males can identify gender based on echolocation call acoustics
(Knörnschild et al. 2012). Although we only played male echolo-
cation calls, it is unlikely that free-tailed bats recognize the gender
of the caller since research has shown that there is a great deal of
within-individual variation in echolocation calls in this species and
no differences between males and females in echolocation call
structure (Gillam & McCracken 2007).
Echolocation-evoked songs were more likely to include all three
of the main song phrases but were shorter than spontaneous songs.
The shorter duration of these songs was not attributable to fewer
numbers of phrases but instead likely reect shorter durations of
the phrases themselves. Echolocation-evoked singing likely noties
passing bats of the presence and location of an occupied and suit-
able day roost, a critical need for migratory bats that may not be
familiar with the local territory. These shorter songs are tailored to
the context in which it they are used because they must rapidly
convey sufcient information to capture the attention of a ying
conspecic that would pass beyond hearing range within 1e2s.
Although these data do not show whether echo-induced songs are
directed exclusively at females or males, these songs may serve
both functions; attracting females and warning males, much like
what is seen in songbirds (Kroodsma & Miller 1996). The function of
spontaneous singing is less clear. Song variation may reect a va-
riety of social contexts in these densely crowded roosts, such
as attracting females to the males location within the roost,
dening or maintaining dominance hierarchies, or promoting
group cohesion.
Our nding that free-tailed bats vary the syntax of their songs in
different social contexts is unique among mammals. Chick-a-dee
calls that have similar combinatorial syntax also show correla-
tions between sequence order and social context (Ficken et al.
1994). However, even songbirds that do not use combinatorial
syntax, per se, and can vary song structure and syntax across
different contexts (Sossinka & Böhner 1980;Dunn & Zann 1996;
Woolley & Doupe 2008;Byers & Kroodsma 2009). This variability
has been closely tied to neural activity in an avian analogue of the
mammalian striatothalamocortical network, the songbirdsante-
rior forebrain pathway (Jarvis et al. 1998,2005;Kao et al. 2005). A
similar network is believed to be important for speech (Jarvis
2004), and, in a pathological state, may underlie a plethora of hu-
man speech disorders (Lieberman 2007). Striatal dopamine sub-
serves vertebrate vocal plasticity and appears to be a key substance
for inducing song variability (Jarvis et al. 1998;Kao et al. 2005). In
mammals, incorporation of the striatothalamic network into the
vocal control circuitry may have been a critical step towards the
evolution of human speech (Doupe & Kuhl 1999;Jarvis 2004;
Jürgens 2009), yet vocal plasticity is rare in mammals with corre-
spondingly little evidence that the basal ganglia participates in
mammalian vocal communication (Jürgens 2009). Unlike most
mammals, however, echolocating bats routinely modulate the
timing and acoustic structure of their vocalizations. Free-tailed bats
show vocalization-related neuronal activity in the dorsolateral
striatum (Schwartz & Smotherman 2011) and pharmacological
manipulations of striatal dopamine profoundly inuence
sensorimotor control of the free-tailed bats voice (Tressler et al.
2011). We have yet to show whether bat song composition is
directly inuenced by basal ganglia activity, but similarities in the
way free-tailed bats and songbirds vary song composition indicate
the two disparate groups may share common design elements
within their song control circuitry. Identifying the neural basis for
these similarities may provide a useful new avenue for exploring
how, when and why vocal plasticity evolved in mammals.
Acknowledgments
We thank our undergraduate research assistants N. Tedford, S.
Trent, K. Rogers and M. Gutierrez for help conducting experiments
and collecting data at the eld sites. We thank B. Earnest and J.
Jarvis for help training bats and maintaining the captive colony, and
P. Narins and W. Metzner for comments on an earlier version of the
manuscript. We are particularly grateful to the Texas A&M
Department of Athletics for providing access to the bats and
allowing us to conduct these experiments within and around their
facilities. This research was supported by Texas A&M University.
Supplementary Material
Supplementary material for this article is available, in the online
version, at http://dx.doi.org/10.1016/j.anbehav.2013.04.002.
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... upsweep-tone) or may occur independently as syllables in their own right (e.g. upsweep; Toth, 2016) A discrete unit of song, surrounded by silences of at least 1 ms (Kanwal et al., 1994;Behr & von Helversen, 2004;Bohn et al., 2008;Bohn et al., 2009;Bohn et al., 2013) A segment of one or more syllables in which the silent period between any two syllables is roughly similar and always less than the total duration of those two syllables (Kanwal et al, 1994;Bohn et al., 2008;Bohn et al., 2013;Wiley, 2018). For our purposes, separated in M. tuberculata by silences of ~20ms The sequence in which phrases are combined. ...
... upsweep-tone) or may occur independently as syllables in their own right (e.g. upsweep; Toth, 2016) A discrete unit of song, surrounded by silences of at least 1 ms (Kanwal et al., 1994;Behr & von Helversen, 2004;Bohn et al., 2008;Bohn et al., 2009;Bohn et al., 2013) A segment of one or more syllables in which the silent period between any two syllables is roughly similar and always less than the total duration of those two syllables (Kanwal et al, 1994;Bohn et al., 2008;Bohn et al., 2013;Wiley, 2018). For our purposes, separated in M. tuberculata by silences of ~20ms The sequence in which phrases are combined. ...
... For our purposes, separated in M. tuberculata by silences of ~20ms The sequence in which phrases are combined. Sequential repetitions of phrases are omitted, so the phrase sequence chirp-trill-trill-chirp belongs to the chirp-trill-chirp song type (Bohn et al., 2013). ...
Thesis
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Short-tailed bats; Mystacina tuberculata; singing behaviour in bats; social organisation
... These features are based on different subunits such as syllables, phrases and bouts of animal vocalizations, and they can reveal the call structure and the rules of syllable ordering in animal vocalizations. However, most studies have used components of these features in one research paradigm (Gadziola et al., 2012;Bohn et al., 2013;Suzuki et al., 2018). For example, Chabout et al. (2015) mainly used the probability of occurrence of a transition type between syllables to compare male mice song syntax depending on social contexts, while Cäsar et al. (2013) compared the types of call sequences between study groups to state that Titi monkey calls varied with predator location and type. ...
... Furthermore, some species have been documented to possess the capacity to vary social calls in response to social cues and behavioural context. For example, Brazilian free-tailed bats, Tadarida brasiliensis, quickly varied song composition to meet the specific demands of different social functions (Bohn et al., 2013). Big brown bats, Eptersicus fuscus, emitted bouts of vocalizations that could be assigned to specific aggressive behaviours (Gadziola et al., 2012). ...
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... Furthermore, numerous studies have suggested that some communication systems of wild and some domestic bird, whale, and primate taxa exhibit syntactic properties, i.e., rules for combining different structures or structure types (Berwick et al. 2011Griesser et al. 2018;Suzuki et al. 2018 Ficken et al. 2000), tits (Paridae; Hailman et al. 1985), chickadees (Poecile;Freeberg 2008;Freeberg and Lucas 2012), true finches (Fringillidae; Riebel and Slater 2003), New World sparrows (Passerellidae; Rose et al. 2004), estrildid finches (Estrildidae; Abe et al. 2011;Beckers et al. 2012;Honda and Okanoya 1999;Katahira et al. 2007;Leonardo 2002;Sturdy et al. 1999;van Heijningen et al. 2009), nightingales and relatives (Luscinia; Hultsch and Todt 1989;Hultsch 1996, 1998), starlings (Sturnidae;Gentner et al. 2006), gulls (Laridae;Beer 1976), bats (Chiroptera; Bohn et al. 2013), mice (Chabout et al. 2015), mongooses (Herpestidae; Fitch 2012), humpback whales (Megaptera novaeangliae; Mercado et al. 2005;Payne and McVay 1971;Suzuki et al. 2006), tamarins (Saguinus;Fitch and Hauser 2004), capuchins (Cebinae;Robinson 1984), and gibbons (Hylobatidae; Clarke et al. 2006;Haimoff 1985;Inoue et al. 2017Inoue et al. , 2020aTerleph et al. 2018). Hurford (2012: 97) comments: "Despite serious underexploitation of combinatoriality, […] whalesong and much birdsong exhibit a hierarchically layered structure formally similar to the hierarchical structure of human syntax." ...
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Recent discoveries of semantic compositionality in Japanese tits have enlivened the discussions on the presence of this phenomenon in wild animal communication. Data on semantic compositionality in wild apes are lacking, even though language experiments with captive apes have demonstrated they are capable of semantic compositionality. In this paper, I revisit the study by Boesch [1991 (Hum Evol 6:81–89] who investigated drumming sequences by an alpha male in a chimpanzee (Pan troglodytes) community in the Taï National Park, Côte d’Ivoire. A reanalysis of the data reveals that the alpha male produced semantically compositional combined messages of travel direction change and resting period initiation. Unlike the Japanese tits, the elements of the compositional expression were not simply juxtaposed but displayed structural reduction, while one of the two elements in the expression coded the meanings of both elements. These processes show relative resemblance to blending and fusion in human languages. Also unlike the tits, the elements of the compositional expression did not have a fixed order, although there was a fixed distribution of drumming events across the trees used for drumming. Because the elements of the expression appear to carry verb-like meanings, the compositional expression also resembles simple verb-verb constructions and short paratactic combinations of two clauses found across languages. In conclusion, the reanalysis suggests that semantic compositionality and phenomena resembling paratactic combinations of two clauses might have been present in the communication of the last common ancestor of chimpanzees and humans, not necessarily in the vocal modality.
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... territorial defence: Behr et al. 2006;Smarsh 2015;Knörnschild et al. 2017; mate attraction: Adams and Snode 2015;contact: Esser and Schmidt 1989;Knörnschild and von Helversen 2008;Arnold and Wilkinson 2011;Carter et al. 2012;Gillam and Chaverri 2012;Montero and Gillam 2015;aggression: Bastian and Schmidt 2008;Jiang et al. 2016;Prat et al. 2016;Walter and Schnitzler 2019;appeasement: Clement and Kanwal 2012;Gadziola et al. 2012;distress: Russ et al. 2004;Carter et al. 2015;Eckenweber and Knörnschild 2016;Huang et al. 2018;Wu et al. 2019). Many social vocalisations have strong functional links to specific behaviours or behavioural contexts (Bohn et al. 2008;Gadziola et al. 2012;Bohn et al. 2013;Prat et al. 2016Prat et al. , 2017, suggesting that such vocalisations can be useful for studying non-vocal behaviours in bats by acoustic proxy. Despite this potential, the use of acoustic signals has largely been limited to presence-absence studies and has rarely been used to investigate social behaviour in bats (but see Andrews et al. 2017). ...
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... Tadarida brasiliensis, appear to have a hierarchical structure composed of composite elements [84] that can vary depending on context [85], population differences indicative of dialects or other evidence suggesting that these songs are learned have not yet been found in this species [38,84]. By contrast, regional differences in acoustic features of male songs have been observed in a different molossid, Nyctinomops laticaudatus, implicating either vocal learning or genetic differentiation [38]. ...
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The comparative approach can provide insight into the evolution of human speech, language and social communication by studying relevant traits in animal systems. Bats are emerging as a model system with great potential to shed light on these processes given their learned vocalizations, close social interactions, and mammalian brains and physiology. A recent framework outlined the multiple levels of investigation needed to understand vocal learning across a broad range of non-human species, including cetaceans, pinnipeds, elephants, birds and bats. Here, we apply this framework to the current state-of-the-art in bat research. This encompasses our understanding of the abilities bats have displayed for vocal learning, what is known about the timing and social structure needed for such learning, and current knowledge about the prevalence of the trait across the order. It also addresses the biology (vocal tract morphology, neurobiology and genetics) and evolution of this trait. We conclude by highlighting some key questions that should be answered to advance our understanding of the biological encoding and evolution of speech and spoken communication. This article is part of the theme issue ‘What can animal communication teach us about human language?’
... Although bird song can be structurally complex, its meaning is thought to be simple; song phrases have a certain function as a whole, facilitating mate attraction, territorial defence or both [20,21]. Similarly, ordering rules have been documented in the vocal sequences of bats [22], mice [23], mongooses [24,25], cetaceans [26,27], gibbons [28] and gorillas [29], but like bird songs, these sequences are typically interpreted as holistic sequences, where the meaning is conveyed by the overall sequence. Thus, the term 'syntax' in animal studies have long been used to signify the rules to combine meaningless elements [6,30]. ...
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Syntax (rules for combining words or elements) and semantics (meaning of expressions) are two pivotal features of human language, and interaction between them allows us to generate a limitless number of meaningful expressions. While both features were traditionally thought to be unique to human language, research over the past four decades has revealed intriguing parallels in animal communication systems. Many birds and mammals produce specific calls with distinct meanings, and some species combine multiple meaningful calls into syntactically ordered sequences. However, it remains largely unclear whether, like phrases or sentences in human language, the meaning of these call sequences depends on both the meanings of the component calls and their syntactic order. Here, leveraging recently demonstrated examples of meaningful call combinations, we introduce a framework for exploring the interaction between syntax and semantics (i.e. the syntax-semantic interface) in animal vocal sequences. We outline methods to test the cognitive mechanisms underlying the production and perception of animal vocal sequences and suggest potential evolutionary scenarios for syntactic communication. We hope that this review will stimulate phenomenological studies on animal vocal sequences as well as experimental studies on the cognitive processes, which promise to provide further insights into the evolution of language. This article is part of the theme issue ‘What can animal communication teach us about human language?’
... Tadarida brasiliensis, appear to have a hierarchical structure composed of composite elements [84] that can vary depending on context [85], population differences indicative of dialects or other evidence suggesting that these songs are learned have not yet been found in this species [38,84]. By contrast, regional differences in acoustic features of male songs have been observed in a different molossid, Nyctinomops laticaudatus, implicating either vocal learning or genetic differentiation [38]. ...
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Human speech involves species‐specific anatomy deriving from the descent of the tongue into the pharynx. The human tongue’s shape and position yields the 1:1 oral‐to‐pharyngeal proportions of the supralaryngeal vocal tract. Speech also requires a brain that can “reiterate”—freely reorder a finite set of motor gestures to form a potentially infinite number of words and sentences. The end points of the evolutionary process are clear. The chimpanzee lacks a supralaryngeal vocal tract capable of producing the “quantal” sounds which facilitate both speech production and perception and a brain that can reiterate the phonetic contrasts apparent in its fixed vocalizations. The traditional Broca‐Wernicke brain‐language theory is incorrect; neural circuits linking regions of the cortex with the basal ganglia and other subcortical structures regulate motor control, including speech production, as well as cognitive processes including syntax. The dating of the FOXP2 gene, which governs the embryonic development of these subcortical structures, provides an insight on the evolution of speech and language. The starting points for human speech and language were perhaps walking and running. However, fully human speech anatomy first appears in the fossil record in the Upper Paleolithic (about 50,000 years ago) and is absent in both Neanderthals and earlier humans.
Book
The voices of birds have always been a source of fascination. Nature's Music brings together some of the world's experts on birdsong, to review the advances that have taken place in our understanding of how and why birds sing, what their songs and calls mean, and how they have evolved. All contributors have strived to speak, not only to fellow experts, but also to the general reader. The result is a book of readable science, richly illustrated with recordings and pictures of the sounds of birds. Bird song is much more than just one behaviour of a single, particular group of organisms. It is a model for the study of a wide variety of animal behaviour systems, ecological, evolutionary and neurobiological. Bird song sits at the intersection of breeding, social and cognitive behaviour and ecology. As such interest in this book will extend far beyond the purely ornithological - to behavioural ecologists psychologists and neurobiologists of all kinds.
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Recent years have seen the development of a theory that claims that human speech involves anatomical and neural specializations that form part of the pattern of hominid evolution. These specializations for human speech differentiate the linguistic ability of anatomically modern Homo sapiens from certain archaic, extinct hominids and from all other living animals. The theory, in brief, claims that the normal adult human supralaryngeal vocal tract has functional, physiologic, properties that yield speech sounds that are better signals for vocal communication than the sounds that are possible to make using the supralaryngeal vocal tract that other living animals have. Evolution is, as Darwin noted, a gradual process and human speech makes use of phonetic contrasts that can be produced by other animals. The theory likewise does not claim that human speech is the key, that is, the sole factor that differentiates human linguistic ability from that of other living animals or archaic hominids. Human speech, however, is an integral part of human linguistic ability and it probably played an important role in channeling the course of human evolution.
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Chick-a-dee calls of the Mexican Chickadee (Parus sclateri) are composed of combinations of three common note types (A, C and D) and one very rare type (B). Calls have the invariant sequence of notes A-B-C-D, where any note type may be omitted, given once or repeated a variable number of times before transiting to the next type. The B and C notes are phonologically similar to the B and C notes of chick-a-dee calls of the Black-capped Chickadee (P. atricapillus), but the A note is markedly different and the D note somewhat different from equivalent notes of the congener. A total of 2,071 calls recorded yielded 60 different call types, and Zipf-Mandelbrot plots show that the call system is "open"; as the sample size is increased new call types will be found without demonstrable bound. In relatively undisturbed contexts (with mate on territory, in fall flocks, alone in fall) birds gave mainly [A][D] calls with lesser numbers of [A] and [C] calls, where brackets indicate variable repetition of note types. In disturbed contexts (mobbing plastic Great Horned Owl, mobbing speaker playing calls of the Northern Pygmy-Owl, observer sitting under the nest cavity) the birds gave more [C] calls with [A][C] as well. In the longest mobbing session to owl calls, birds gave mainly [A] calls when approaching, switched to [C] calls while flying about the speaker, and then resumed [A] calls and moved off when the playback was stopped. Outside of human language, this is the second truly combinatorial system of vocal communication found in animals, the first being chick-a-dee calls of the Black-capped Chickadee. This study provides the first data substantiating quantitative differences in calls from different contexts, an important step toward understanding what kinds of information combinatorial chick-a-dee calls encode.
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We describe vocalizations of Black-chimed Hummingbirds (Archilochus alexandri) recorded during agonistic encounters at feeders. Calls are composed of one to five different note-types that comprise a recombinatorial system exhibiting syntax. A Markov analysis revealed non-random ordering of note-types. The distribution of call-types (unique combinations of notes) illustrates openness; the number of call-types increases as more calls are sampled. Constraints on call length occur that are related to the length of individual note-types; shorter note-types are more common in calls with more notes. No sex differences occurred in the call-types with the exception of the Z note which occurred more often in male calls. The agonistic vocalizations of these hummingbirds demonstrate a level of vocal complexity comparable to songs of many passerines. We compare the vocalizations of the Black-chimed Hummingbird with studies of Anna's Hummingbird (Calypteanna) and point out major differences in repertoire organization. Marked similarities occur between organization of calls in certain chickadees (Pants) and that of the Black-chimed Hummingbird. This finding is surprising in view of their phyletic differences, but may reflect certain underlying constraints on the organization of avian vocalizations.