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Alarm calls evoke a visual search image of a predator in birds

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One of the core features of human speech is that words cause listeners to retrieve corresponding visual mental images. However, whether vocalizations similarly evoke mental images in animal communication systems is surprisingly unknown. Japanese tits (Parus minor) produce specific alarm calls when and only when encountering a predatory snake. Here, I show that simply hearing these calls causes tits to become more visually perceptive to objects resembling snakes. During playback of snake-specific alarm calls, tits approach a wooden stick being moved in a snake-like fashion. However, tits do not respond to the same stick when hearing other call types or if the stick's movement is dissimilar to that of a snake. Thus, before detecting a real snake, tits retrieve its visual image from snake-specific alarm calls and use this to search out snakes. This study provides evidence for a call-evoked visual search image in a nonhuman animal, offering a paradigm to explore the cognitive basis for animal vocal communication in the wild.
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Alarm calls evoke a visual search image of a predator
in birds
Toshitaka N. Suzuki
a,b,1
a
Center for Ecological Research, Kyoto University, Otsu, 520-2113 Shiga, Japan; and
b
Department of Evolutionary Studies of Biosystems, Graduate
University for Advanced Studies, Hayama, 240-0193 Kanagawa, Japan
Edited by Asif A. Ghazanfar, Princeton University, Princeton, NJ, and accepted by Editorial Board Member Marlene Behrmann December 29, 2017 (received for
review October 30, 2017)
One of the core features of human speech is that words cause
listeners to retrieve corresponding visual mental images. How-
ever, whether vocalizations similarly evoke mental images in
animal communication systems is surprisingly unknown. Japanese
tits (Parus minor) produce specific alarm calls when and only when
encountering a predatory snake. Here, I show that simply hearing
these calls causes tits to become more visually perceptive to ob-
jects resembling snakes. During playback of snake-specific alarm
calls, tits approach a wooden stick being moved in a snake-like
fashion. However, tits do not respond to the same stick when
hearing other call types or if the sticks movement is dissimilar
to that of a snake. Thus, before detecting a real snake, tits retrieve
its visual image from snake-specific alarm calls and use this to
search out snakes. This study provides evidence for a call-evoked
visual search image in a nonhuman animal, offering a paradigm to
explore the cognitive basis for animal vocal communication in
the wild.
animal communication
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cognition
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language
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referentiality
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visual mental image
In human speech, words referring to a specific object (e.g.,
moon) evoke a visual mental image in listeners or readers (1,
2). In cognitive and neural sciences, visual mental imagery can be
defined as representations and the accompanying experience of
sensory information without a direct external stimulus (3, 4).
Thus, at the behavioral level, receivers who retrieve a visual
mental image from referential words are expected to enhance
their detection of a target object (5, 6). In nonhuman animal
communication systems, many key, language-like features have
been demonstrated (1, 7), but whether animal signals also evoke
mental images in receivers is surprisingly unknown (810). Dis-
covering evidence for the retrieval of visual mental images from
vocal signals in animals would have fundamental implications for
our understanding of animal cognition, neural mechanisms, and
the adaptation and evolution of linguistic capabilities (1, 2).
Here, using a paradigm, I provide experimental evidence that
vocalizations in a nonhuman animal evoke a visual mental image
of a referent.
Call-evoked visual mental images may have evolved in animals
that produce unique calls to specific objects in their environment
(11, 12). One candidate species is the Japanese tit (Parus minor),
which produces acoustically distinct alarm calls in response to
different predators (13). The calls that tits give when and only
when encountering predatory snakes are considered function-
ally referentialbecause they elicit specific antisnake behaviors
in receivers (1416) (Fig. 1A). For example, when incubating
eggs in the nest, adults respond to snake-specific alarm calls by
immediately escaping out of the nest cavity, allowing them to
evade attacks from snakes which can invade the cavity (16).
When outside of the nest cavity, they respond to snake-specific
alarm calls by looking down at the ground nearby their nest tree,
which suggests an adaptive behavior to locate approaching
snakes (15). In addition to snake-specific alarm calls, tits have
evolved another call type used for a wide range of predator types,
including avian and mammalian predators (13) (Fig. 1B). In re-
sponse to these general alarm calls, receivers approach the sound
source and scan the surroundings (17), but do not show any
specific behaviors to defend themselves against snakes (15, 16).
Based on these previous studies, I hypothesized that snake-
specific alarm calls evoke a visual search image of a snake in tits.
A key prediction of this hypothesis is that receivers are primed to
detect snakes when hearing snake-specific alarm calls. However,
to provide evidence for visual mental imagery, individuals should
be primed to detect snakes even in the absence of real snakes,
since simply seeing a snake may directly trigger its mental image
(3, 4). To account for this possibility, I designed a field experi-
ment to test whether snake-specific alarm calls prime tits to
perceive an otherwise indistinct object as a real snake. If the
hypothesis is correct, tits are expected to show a specific behavior
toward a snake-like object when and only when hearing these
calls. Alternatively, if responses to snake-specific alarm calls are
not dependent on visual search images, hearing the calls should
not specifically improve the detection of a snake-like object, but
would simply evoke a stereotyped behavior (e.g., looking down at
the ground). I tested the responses of free-living Japanese tits to
specific associations between different call types and visual
stimuli (snake-like or nonsnake-like objects) during their early
breeding season.
Results and Discussion
First, I attracted an individual, focal tit by broadcasting snake-
specific alarm calls from a speaker hung in a tree. Immediately
after the focal tit flew to the tree and perched on a tree branch
Significance
In human speech, words often cause listeners to retrieve visual
mental images of target objects. In nonhuman animal com-
munication systems, many key, language-like features have
been demonstrated, but there is still no evidence that animal
signals evoke mental images of objects in receivers. Japanese
tits produce specific alarm calls when encountering a predatory
snake. Here, I show that simply hearing these calls causes tits
to become more visually perceptive to objects resembling
snakes (moving sticks). This result indicates that before having
detected a real snake, tits retrieve its visual image from snake-
specific alarm calls and uses this to search out snakes. This
study provides evidence for a call-evoked visual search image
in a nonhuman animal.
Author contributions: T.N.S. designed research, performed research, analyzed data, and
wrote the paper.
The author declares no conflict of interest.
This article is a PNAS Direct Submission. A.A.G. is a guest editor invited by the
Editorial Board.
Published under the PNAS license.
1
Email: toshi.n.suzuki@gmail.com.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1718884115/-/DCSupplemental.
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around the speaker, I presented a short stick (18-cm length,
1.5-cm diameter) cut from a dead branch by pulling it up for 1 m
along the tree trunk, using a thin string that I manipulated from a
distance (Fig. 2A; Experiment 1). This movement imitates the
movement of a snake, as no animals in the study area other than
bird-eating snakes (Japanese rat snakes, Elaphe climacophora)
move up a tree trunk in this way. To control for the possibility
that simply perceiving any threating signal causes tits to respond
to the stick movement, I also tested their responses to the stick
during playback of general alarm calls. If tits retrieved the visual
mental image of a snake from snake-specific alarm calls, then
they are expected to exhibit a greater response to the moving
stick when hearing snake-specific calls than when hearing gen-
eral alarm calls.
Responses of Japanese tits to the stick differed according to
the types of alarm calls they heard (Fig. 3A). When hearing
snake-specific alarm calls, focal individuals consistently flew to-
ward and approached within 1 m of the stick moving snake-like
up a tree trunk and inspected the surroundings (92%, 11/12 tri-
als; Movie S1). In some cases (58%, 7/12 trials), they also
approached within 0.5 m of the stick. In contrast, when hearing
general alarm calls, they rarely approached within 1 m of the
moving stick (8%, 1/12 trials) (Fishers exact probability test,
1m:P<0.001). Thus, in response to snake-specific alarm calls
individuals approached the stick, but in response to general
alarm calls they did not approach the stick.
Although this result supports the hypothesis, there remains the
possibility that tits only detect urgency information from both
alarm call types (e.g., snake-specific alarm calls convey greater
urgency than general alarm calls), thus exhibiting different re-
sponses to the stick when hearing different alarm calls. If this is
true, tits are expected to approach the stick more often when
hearing any alarm call type, than when hearing nonalarm calls.
To account for this possibility, I investigated titsresponses to the
stick during the playback of recruitment calls (Fig. 1C). Re-
cruitment calls are produced to attract conspecific receivers in
nonpredatory contexts, such as when recruiting a mate to the
nest or food, and do not evoke any alert behavior (17).
Although general alarm calls do convey more urgency than
recruitment calls (17), tits responded similarly to the stick during
playbacks of these two call types (Fishers exact probability test,
1m:P=1.0; Fig. 3A). However, tits are less likely to approach
the stick during playback of recruitment calls (17%, 2/12 trials)
compared with the playback of snake-specific alarm calls (Fish-
ers exact probability test, P<0.001). Thus, titsresponses to the
stick are not simply driven by the urgency information encoded
0
5
10
15
20
Frequency (kHz)
Snake-specific alarm call
0
5
10
15
20
Frequency (kHz)
General alarm call
0
5
10
15
20
Frequency (kHz)
Recruitment call
A
B
C
0.5 s
Fig. 1. Sound spectrograms of Japanese tit vocalizations. (A) Snake-specific
alarm call. (B) General alarm call. (C) Recruitment call.
burhs a no gnigniwSdnuorg eht no gniggarDMoving up a tree trunk CBA
2 tnemirepxE1 tnemirepxE
Speaker Stick
Fig. 2. Schematic representation of experimental setup. (A) In Experiment 1, tits were exposed to a stick moving snake-like up a tree trunk immediately after
they approached within 2 m above the speaker. (B) In Experiment 2, tits were exposed to another snake-like movement of a stick: dragging on the ground.
(C) In Experiment 2, tits were also exposed to nonsnake-like movement of a stick: swinging on a low shrub.
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in the calls, but rather, the referential information encoded in
the snake-specific alarm calls.
These results demonstrate that snake-specific alarm calls
specifically prime tits to respond to a stick moving in a snake-like
way, suggesting that they retrieve a visual search image of a
snake from these calls. However, another possible explanation is
that snake-specific alarm calls cause receivers to approach any
object moving in the environment without evoking a specific
search image of a snake. According to the hypothesis that snake-
specific alarm calls evoke a snake-specific search image, tits are
expected to approach a stick when it moves in a snake-like way in
a variety of contexts, such as on the ground. In addition, tits
should not respond to a stick moving in a pattern that is in-
consistent with a snake, such as swinging. To test these possi-
bilities, I conducted an additional experiment to investigate tits
responses to different combinations of alarm calls and stick
movement patterns (being moved in a snake-like fashion on the
ground or a nonsnake-like fashion being swung from a low
shrub; Experiment 2; Fig. 2 Band C).
Japanese tits frequently approached within 1 m of a stick
dragged on the ground and inspected the surroundings during
the playback of snake-specific alarm calls (83%, 10/12 trials). In
several cases (25%, 3/12 trials), they also approached within
0.5 m of the stick. However, they never approached the snake-
like movement of a stick when hearing general alarm calls (0%,
0/12 trials) (Fishers exact probability test, 1 m: P<0.0001) (Fig.
3B). Moreover, tits rarely approached a stick that was swung in a
nonsnake-like motion from a low shrub when hearing either
snake-specific (8%, 1/12 trials) or general alarm calls (0%,
0/12 trials) (Fishers exact probability test, 1 m: P=1.0) (Fig.
3C). In combination with the first experiment, these results
demonstrate that tits that heard snake-specific alarm calls did
not simply turn their attention to any moving object. Instead they
searched for and focused on snake-like objects, regardless of
their spatial position. Since snake-specific alarm calls caused tits
to specifically approach a stick only if it was moved in a snake-
like fashion, these calls did not simply evoke a stereotyped be-
havior. Thus, I conclude that Japanese tits retrieve a visual
search image of a snake from snake-specific alarm calls without
needing to see a real snake.
Retrieving a visual search image when hearing calls could
provide adaptive benefits to receivers. First, the selective re-
trieval of a snake search image from snake-specific alarm calls
would allow tits to focus on snakes and not on other predators,
which should increase the efficiency of finding snakes. Upon
detecting a real snake, tits approach the snake closely and hover
over it, spreading their wings and tail, which might function in
deterring it from predatory attacks (18). In this study, tits
approached a snake-like moving stick during the playback of
snake-specific alarm calls, but did not exhibit such mobbing be-
havior, suggesting that they may realize that the stick is not a real
snake once they get close enough. Secondly, the retrieval of a
snake image from snake-specific alarm calls would allow tits to
alter their responses according to context. This is supported by
previous studies showing that adult tits respond differently to
snake-specific alarm calls depending on whether they are inside or
outside of their nest cavities (15, 16). Thus, the need for the ef-
ficient detection of external referents and for context-dependent
shifts in responses might select for the evolution of communica-
tion through visual mental imagery.
This study provides experimental evidence for the retrieval of
a visual search image from a specific call type in a nonhuman
animal. Using either habituationdishabituation or expectation
of violation paradigms, previous studies have shown that several
nonhuman primates and birds associate specific call types with
related stimuli (1922), suggesting that these animals may form
mental representations of external objects. However, since most
of these studies have investigated the specific associations be-
tween two auditory stimuli (i.e., alarm calls and predator vocal-
izations) (1921), it has been a long-standing challenge to
determine whether specific calls evoke a visual mental image in
animals (1, 2). Using an object that somewhat resembles the
referent but does not solely evoke a specific behavior, it could be
tested whether subjects become more visually perceptive to that
object when hearing specific calls. Despite once being considered
a uniquely human trait (23), the integration of cross-modal in-
formation has now been documented for a wide variety of ver-
tebrates, such as birds (24, 25) and mammals (2629). While
such cross-modal performance has been shown to enhance rec-
ognition of individual identity or the emotional state of signalers
BA
0
25
50
75
100
Recruitment General alarm Snake alarm
Movin
g
up a tree trunk
Approa ch (%)
0
25
50
75
100
General Snake General Snake
Dra
gg
in
g
on the
g
round Swin
g
in
g
on a shrub
Approach (%)
Experiment 2Experiment 1
Fig. 3. Responses of Japanese tits to a stick. (A) Experiment 1. Tits approached a stick moving up a tree trunk during the playback of snake-specific alarm
calls, but rarely during the playbacks of general alarm calls and recruitment calls. Sample size: n=36 trials. Each focal bird was exposed to only one treatment,
giving n=12 trials per treatment. (B) Experiment 2. Tits approached a stick moving on the ground during the playback of snake-specific alarm calls, but not
during the playback of general alarm calls. However, they rarely approached the stick when its movement (swinging) was dissimilar to a snake movement
regardless of the type of alarm call they heard. Sample size: n=48 trials. Each bird was exposed to only one treatment, giving n=12 trials per treatment.
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(2429), my results reveal that cross-modal integration of audi-
tory and visual stimuli can be involved in referential communi-
cation in animals. In light of this discovery, future research will
no doubt begin to uncover the ecological importance of visual
mental imagery in animal vocal communication, as well as the
developmental and neural mechanisms underlying this cognitive
sophistication.
Materials and Methods
Study Site and Subjects. Experiments were conducted on Japanese tits (P.
minor) in mixed deciduousconiferous forests in Nagano and Gunma
(36°1925N, 138°2739E), Japan. In this study site, there were three
species of snakes, including Japanese rat snakes, Japanese forest rat snakes
(E. conspicillata), and tiger keelbacks (Rhabdophis tigrinus). Only Japanese
rat snakes climb up trees and prey on birds including eggs, young, and
adults. Experiments were conducted between May 18 and May 30, 2017
(Experiment 1) and April 22 and May 12, 2014 (Experiment 2), during the
early breeding season of tits. Within each experiment, trials were conducted
at different sites (n=36 in Experiment 1, n=48 in Experiment 2), which
were separated by at least 350 m. This distance was enough to ensure that
independent data were collected from different individuals, which was
confirmed by observations of color-ringed Japanese tits in a previous study
(30). Trials took place under calm and dry weather between 0830 and
1600 hours (Japan Standard Time).
Experimental Stimuli. Sticks (n=12; 18-cm length, 1.5-cm diameter) were cut
from dead branches and were then connected to a thin, black string. Play-
back stimuli for the three call types were constructed from previous re-
cordings of Japanese titsvocalizations (13, 14) and were edited by using
Adobe Audition 3.0 software (Adobe Corporation). For each playback ex-
emplar, one call was chosen from an individual on the basis of sound quality
(i.e., when the signaler was close to the microphone and there was low
background noise) and was repeated in a sound file at a rate of five calls per
12 s (one call every 2.4 s), imitating a natural calling rate in Japanese tits (13,
14). Snake-specific alarm calls are composed of a single type of note,
whereas general alarm calls can vary subtly with their note composition (13).
I used general alarm calls composed of four types of notes (a string of A, B,
and C notes followed by 710 D notes) since this combination is a typical
composition of general alarm calls and recruits individuals to scan for danger
(17). Recruitment calls are composed of 710 D notes, which recruit indi-
viduals to nondangerous situations (17). Previous playback studies have
shown that all three of the calls attract Japanese tits to within 2 m of the
speaker (15, 17, 31). I filtered out low-frequency (<1 kHz) noise and ampli-
fied all of the calls to be played back at a standardized volume (75 dB re:
20 μPa at 1 m from the speaker measured using an SM-325 sound-level
meter; AS ONE Corporation). I saved all sound files in .WAV format (16-bit
depth, 48.0-kHz sampling rate) to an SD memory card. For each treatment,
12 exemplars were constructed using the calls of 12 individuals that had
been recorded with an LS370 parabolic microphone (Fuji Planning Cor-
poration) connected to an R-09HR digital audio recorder (16-bit depth,
48.0-kHz sampling rate; Roland Corporation) (13, 14).
Experiment 1. This experiment investigated the responses of tits to a stick
moving up a tree trunk during the playback of snake-specific alarm calls,
general alarm calls, or recruitment calls. At each experimental site, an AT-
SPG50 speaker (Audio-Technica Corporation) was hung from a tree branch at
1.5 ±0.1 m above the ground. The speaker was connected to an R-09HR
digital audio recorder using EXC-12A extension cords (JVC KENWOOD Cor-
poration) to control the playbacks from an observation position 10 m away
from the speaker tree. A stick was fixed at a height of 1.1 ±0.2 m (mean ±
SD, n=24) on the trunk of a different tree. This tree was carefully chosen
with the following criteria: (i) it allowed the stick to be pulled up the tree
trunk in a straight line to imitate a snake moving up the trunk, (ii) it allowed
the stick to be visible from the position of the speaker, ensuring that an
approaching, focal bird was exposed to the stick, and (iii ) it allowed the stick
to be located at a distance of 3.2 ±0.2 m (mean ±SD, n=36) from
the speaker.
Playbacks were started when no birds were visible around the speaker tree
and no birds were calling. When a focal tit flew to the speaker tree and
approached within 2 m above the speaker where it could see the stick, the
movement of the stick was initiated by pulling up the thin string 20 cm and
continually repeating this movement five times for 12 s. I then recorded
whether the focal tit flew directly toward the moving stick during the first
24 s. Observations were made 10 m from the tree with the stick and the
trials were video-recorded using a GZ-EX350 digital video camera (JVC
KENWOOD Corporation). After each trial, I used a tape measure to measure
the minimum approach distance of the focal bird to the stick. I confirmed
the exact location at which the focal bird made the closest approach by
checking the video recording at each experimental site. When the focal tit
flew toward the moving stick, it also approached within 1 m of the stick, so I
used this distance to determine approach behavior. In consideration for the
possibility of observer bias in behavioral data (32), I conducted an in-
terobserver reliability test with a second rater who was naive to the hy-
pothesis but had been accustomed to observing Japanese tit behavior. The
second rater observed randomly selected video clips (n=18, 50% of the
trials) and estimated whether tits approached within 1 m of the stick or not.
The results obtained from the author and the second rater showed a high
degree of agreement, indicating that there was no observer bias (kappa
statistic of 1.0) (32).
The order of trials (snake alarm, general alarm, and recruitment calls) was
counterbalanced across treatments so that responses to all treatments were
observed under largely similar conditions. In seven trials, the first bird to
approach the call playback was from a heterospecific species, such as a coal tit
(Periparus ater)(n=6) or a willow tit (Poecile montanus)(n=1). To account
for the possibility that Japanese tits copied the behavior of these other birds,
I only used the data from instances where the first individual to approach
the speaker was a Japanese tit. Otherwise, I repeated the same treatment at
the next site. Unique exemplars of calls (n=12) were used for each trial to
completely avoid pseudoreplication (33). Unique exemplars of sticks (n=12)
were also used for each trial within each treatment.
Experiment 2. This experiment investigated the responses of tits to two types
of stick movements (along the ground and swinging on a shrub) in combi-
nation with playbacks of either snake-specific or general alarm calls. As in
Experiment 1, an AT-SPG50 speaker was hung from a tree branch at 1.4 m
above the ground, and was connected to an R-09HR digital audio recorder
using EXC-12A extension cords. For the snake-like movement along the
ground, the stick was positioned on the ground at a distance of 2.5 m from
the speaker, and the string was extended from the stick to the observation
position to control the movement of the stick from a distance. To generate
the nonsnake-like swinging movement, the stick was attached to a small
shrub (1.0 ±0.2 m high, mean ±SD, n=24) at a distance of 2.5 m from the
speaker and the string was extended to the observation position, so that I
could swing the stick from a distance.
Playbacks were started when no birds were visible around the speaker tree
and no birds were calling. When a tit flew to the speaker tree and approached
within 2 m above the speaker where it could see the stick, the movement of
the stick (dragging on the ground or swinging on a shrub) was initiated by
pulling the thin string 20 cm and continually repeating this movement five
times for 12 s. I then recorded whether the focal tit approached within 1 m of
the moving stick during the first 24 s. I also measured the minimum distance at
which the focal tit approached the stick, as in Experiment 1. Interobserver
reliability tests between the author and a second naive rater were also
conducted for these analyses using randomly selected video clips (n=12 for
each movement type, 50% of the trials). The results showed a high degree of
agreement between the two raters, indicating that there was no observer
bias (kappa statistic: 1.0 for both) (32).
Trials were conducted in 12 blocks, with all 4 treatments (2 call types ×
2 movement types) presented in a randomized order. As in Experiment 1,
unique call exemplars and unique sticks were used for each block to avoid
pseudoreplication (33). When the first bird to approach an alarm call play-
back was from a heterospecific species (n=40 trials), I repeated the same
treatment at the next site.
Statistical Analysis. Fishers exact probability tests were used to compare the
probability of approach to the movement of the stick. All tests were two-
tailed, and statistical significance was set at α=0.05. When making multiple
comparisons, a false discovery rate control was applied to adjust Pvalues
(34). All of the statistical analyses were performed in R (35) using the
stats package.
Ethics Statement. All experiments were performed in accordance with rele-
vant guidelines and regulations. All experimental protocols were approved
by the Animal Care and Use Committees at The Graduate University for
Advanced Studies, and adhered to the Guidelines for the Use of Animals of
the Association for the Study of Animal Behaviour/Animal Behavior Society
(36). This research was performed with permission from the Ministry of the
Environment and the Forestry Agency of Japan.
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ACKNOWLEDGMENTS. I am grateful to Craig Barnett, Michael Griesser, and
Daizaburo Shizuka for helpful comments on earlier versions of the manuscript,
and to Alexis C. Billings and David Wheatcroft for valuable comments on the
manuscript. I also thank the editor and two anonymous reviewers for their
helpful suggestions in revising the manuscript. This work was supported by Japan
Society for the Promotion of Science KAKENHI Grant 25-3391 and 16752305.
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Suzuki PNAS
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February 13, 2018
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vol. 115
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no. 7
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1545
ECOLOGY PSYCHOLOGICAL AND
COGNITIVE SCIENCES
... For example, in several species of birds and mammals, distinct alarm calls in response to the presence of predators have been observed to induce audience animals to exhibit adaptive evasion responses according to the nature of predator movements (reviewed in Suzuki, 2016;Townsend & Manser, 2013). Moreover, carefully designed playback experiments suggest that audience animals are not simply responding to calls in a fixed manner (Clay & Zuberbühler, 2011;Evans & Evans, 2007;Seyfarth & Cheney, 1990;Slocombe & Zuberbühler, 2005;Suzuki, 2018Suzuki, , 2020Zuberbühler, 2000;Zuberbühler et al., 1999). For example, in a field experiment (Seyfarth & Cheney, 1990), vervet monkeys (Cercopithecus aethiops) repeatedly heard playbacks of either conspecific alarm calls or alarm calls of a sympatric bird species (superb starlings: Spreo superbus). ...
... Another line of evidence supporting this claim comes from cross-modal matching experiments, in which participants are sequentially presented with auditory and visual stimuli, and observed for spontaneous responses to the visual referents of the auditory stimuli (Suzuki, 2016). In studies of wild tits, birds approached a wooden stick that simulated snake-like movements only when they heard snake-specific alarm calls of conspecifics (Suzuki, 2018;or heterospecifics: Suzuki, 2020) but not when they heard an irrelevant call, or when the stick exhibited irrelevant movement (Japanese great tits [Parus minor]: Suzuki, 2018; coal tits [Periparus ater]: Suzuki, 2020). Thus, tits appeared to be primed to detect snakes when they heard snake-specific calls. ...
... Thus, it is possible that chimpanzees may have compared the presented options and inferred only the most relevant item among them (Adachi et al., 2007; for a relevant finding with human infants, see Wu et al., 2017). Future experiments in which an auditory stimulus is played before showing the visual stimulus may be useful to more strictly examine whether calls evoke a representation of a specific object (Suzuki, 2016(Suzuki, , 2018. ...
Article
Calls of several species of nonhuman animals are considered to be functionally referential. However, the cognitive mechanisms underlying audience behaviors remain unclear. This study used an audiovisual cross-modal preferential-looking paradigm to examine whether captive chimpanzees spontaneously associated a conspecific call with images of a corresponding item. Chimpanzees were presented with videos of snakes and fruit side-by-side while hearing playbacks of alarm calls, food-associated calls, or no sound (as a baseline condition). Chimpanzees looked at videos of snakes for longer when hearing alarm calls compared with food calls or baseline. However, chimpanzees did not look at videos of fruit for longer when hearing food calls compared with baseline. An additional experiment tested whether chimpanzees' gaze bias to the snake videos was driven by negative affective states in general via affect-driven attention biases. When chimpanzees were presented with the same snake and fruit videos while hearing playbacks of conspecific screams or no sound, they exhibited no gaze bias for snake videos. These results suggest that chimpanzees spontaneously associated alarm calls with images of a potential threat in a preferential-looking experiment and that this response was not simply driven by an affective state matching process. These findings should be interpreted in consideration of a procedural limitation related to pseudoreplication in the experimental stimuli. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
... Alarm signals and cues are crucial to survival and vary greatly across species. They can signal predation events or predator activity to prey conspecifics, and thus help to avoid predators and decrease predation risk (Gonzalo et al. 2010;Mahr and Hoi 2018;Suzuki 2018). Acoustic alarm signals are conspicuous and are widely used in different taxa (Caro 2005;Casar and Zuberbuhler 2012;Toledo et al. 2015). ...
Article
Full-text available
Alarm signals and cues are crucial to animal survival and vary greatly across species. Eavesdropping on heterospecific alarm signals and cues can provide eavesdroppers with information about potential threats. In addition to acoustic alarm signals, evidence has accumulated that chemical alarm cues and disturbance cues can also play a role in alerting conspecifics to potential danger in adult anurans (frogs and toads). However, there is very little known about whether disturbance cues are exploited by heterospecifics. In the present study, we conducted a binary choice experiment and a prey chemical discrimination experiment, respectively, to test the responses of a sympatric anuran species (red webbed treefrogs, Rhacophorus rhodopus) and a sympatric predator species (Chinese green tree vipers, Trimeresurus stejnegeri) to disturbance odors emitted by serrate-legged small treefrogs (Kurixalus odontotarsus). In the binary choice experiment, we found that the presence of disturbance odors did not significantly trigger the avoidance behavior of R. rhodopus. In the prey chemical discrimination experiment, compared with odors from undisturbed K. odontotarsus (control odors) and odorless control, T. stejnegeri showed a significantly higher tongue-flick rate in response to disturbance odors. This result implies that disturbance odor cues of K. odontotarsus can be exploited by eavesdropping predators to detect prey. Our study provides partial evidence for heterospecific eavesdropping on disturbance cues and has an important implication for understanding heterospecific eavesdropping on chemical cues of adult anurans.
... Our results suggest that social interspecific learning and calls similarity between house wrens and great tits are not the main recognition mechanisms explaining the responses of great tits to house wren calls. Another explanation is that great tits have a mental representation/or abstract concept of urgency following a simple rule "higher calling rate, higher threat" and respond accordingly (Randler, 2012;Suzuki, 2018). Finally, additional experimental work, particularly responses of young birds to playbacks of heterospecific calls with high-and low-calling rates, is required to explore the developmental mechanisms of responsiveness to urgency in heterospecific alarm calls. ...
Article
Many species of birds use alarm calls to signal information about predators, including the level of threat. Previous playback experiments suggest that the urgency response towards heterospecific calls is phylogenetically conserved, notably in the Paridae family. Using playback experiments conducted on European great tits (Parus major), we tested whether this species perceives information about urgency in mobbing calls produced by an allopatric non‐Paridae species, the Southern house wren (Troglodytes aedon bonariae), by broadcasting calls with high‐calling rate (high threat) and calls with low‐calling rate (low threat). We found that great tits tend to approach the loudspeaker during playbacks of calls with high‐calling rate more often than during playbacks of calls with low‐calling rate. Female great tits gave more calls during playbacks of calls with high‐calling rate than during playbacks of calls with low‐calling rate, whereas there was no significant difference in the number of calls given by males between playbacks of calls with high‐ and low‐calling rates. Thus, our results suggested that great tits perceived the urgency message encoded in calls given by an allopatric non‐Paridae species. Using playback experiments conducted on European great tits, we tested whether this species perceives information about urgency in mobbing calls produced by an allopatric non‐Paridae species, the Southern house wren, by broadcasting calls with high‐calling rate (high threat) and calls with low‐calling rate (low threat). We found that tits tend to approach the loudspeaker during playbacks of calls with high‐calling rate more often than during playbacks of calls with low‐calling rate. Moreover, females gave more calls during playbacks of calls with high‐calling rate than during playbacks of calls with low‐calling rate.
... As expected, we found that male disturbance odors can trigger an avoidance response by females, demonstrating that disturbed male odors of K. odontotarsus can act as an alarm cue for conspecifics. Many vertebrates use signals or cues to warn con-or heterospecifics of potential predation risk (Schmitt et al. 2016;Oliveira et al. 2017;Haapakoski et al. 2018;Suzuki 2018). For example, Ruiz-Monachesi and Labra (2020) reported that conspecific distress calls triggered a reduction in activity in weeping lizard (Liolaemus chiliensis). ...
Article
Full-text available
Mate choice in frogs depends heavily on acoustic communication, and females in many species possess an inherent preference for longer and/or more complex calls. Recently, it has become clear that conspecific chemical cues can also be useful in attracting potential mates in anuran species. However, how conspecific chemical cues influence mate choice decisions when paired with acoustic signals remains less clear. In the present study, we conducted three experiments to investigate whether and how male odor cues affect female choice decisions in the absence or presence of acoustic signals in serrate-legged small treefrogs (Kurixalus odontotarsus). We found that disturbance odors alone can trigger avoidance behavior of females, suggesting that the odors of disturbed K. odontotarsus can act as an alarm cue for conspecifics. Females also avoided disturbance odors in the presence of advertisement calls, except for calls with five notes. In addition, females preferred calls with two notes to calls with four notes when the latter was paired with disturbance odors. In contrast, female choice decisions were not affected by the odors of undisturbed males, either in the absence or the presence of advertisement calls. Our results indicate that disturbance odors can influence, or even reverse, mate choice by females for acoustic signals. Significance statement In addition to acoustic signals, chemical cues can also be used in close-range communication in some anuran species. In the present study, we investigated how female Kurixalus odontotarsus use male chemical cues and/or acoustic signals during the mate choice process. We demonstrate that male disturbance odors can act as an alarm cue to trigger the avoidance behavior of females. Furthermore, this alarm cue can even reverse mate choice by females for acoustic signals. Our study highlights the importance of integrating multisensory signals and cues in mate choice decisions and has important implications for understanding chemical communication in anurans.
... Its graded behavioral response that differs among predator types, and threats allows for straightforward experiments that ask the focal individual how they perceive the predator, making it useful for experiments addressing predator recognition and categorization. Different species can and do differentiate between different predators within and between taxonomic categories (Griesser, 2009;Suzuki, 2014Suzuki, , 2018Templeton, Greene, & Davis, 2005), predator behaviors and states (Griesser, 2008), and predator features, if they use any to make these differentiations of exposure to a new stimulus alongside a simulated mobbing event has shown that individuals can learn to recognize new predators or new mobbing calls (Griffin, 2004), what aspects of mobbing are needed to make these new connections (Griffin, 2004), and the degree to which new information about novel or known stimuli can override personal experience (Curio et al., 1978a;Vieth et al., 1980). Nonetheless, we still lack an understanding of many fundamental aspects of mobbing. ...
Article
Mobbing is an important anti-predator behavior where prey harass and attack a predator to lower the immediate and long-term risk posed by it, warn others, and communicate about the predator's threat. While this behavior has been of interest to humans since antiquity, and aspects of mobbing have been well researched for the past 50 years, we still know little about its ecology and the evolutionary pressures that gave rise to this widespread anti-predator behavior. In this review, we explore what mobbing is, how it is used, what its functions are thought to be, and its use as a proxy for cognition, before providing suggestions for specific future avenues of research to improve our understanding of the ecology and evolution of mobbing. Here is a share link which allows free access and download until May 03, 2022. https://authors.elsevier.com/a/1eksFEsvggd%7EV
... Such calls can contain specific information as to the identity of the predator. These calls evoke a search image of the specific predator in the receiver which cannot be evoked by other alarm calls (Japanese tit, Parus minor) [28]. Some species even eavesdrop on the alarm calls of other, sympatric species with which they share predators. ...
Article
Full-text available
Interest in studying cognitive ecology has moved the field of animal cognition into the wild. Animals face many challenges such as finding food and other resources, avoiding and deterring predators and choosing the best mate to increase their reproductive success. To solve these dilemmas, animals need to rely on a range of cognitive abilities. Studying cognition in natural settings is a powerful approach revealing the link between adaptive form and biological function. Recent technological and analytical advances opened up completely new opportunities and research directions for studying animal cognition. Such innovative studies were able to disclose the variety in cognitive processes that animals use to survive and reproduce. Cognition indeed plays a major role in the daily lives of wild animals, in which the integration of many different types of information using a diverse range of cognitive processes enhances fitness.
... Such an acoustic analysis cannot, unfortunately, reveal whether a particular vocalisation is semantic or not (cf. Seyfarth et al., 1980a, b;Suzuki, 2012Suzuki, , 2015Suzuki, , 2016Suzuki, , 2018Suzuki, , 2019. Leroux et al.'s (2021) assumption is further vague as they propose no semantic content for the putatively semantic pant-hoots. ...
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I read with great interest the study by Leroux et al. [(2021) Anim Behav 179, 41–50] who investigated the nature of pant-hoot–food-call combinations in a community of wild chimpanzees (Pan troglodytes schweinfurthii) at the Budongo Conservation Field Station, Budongo Forest, Uganda. The authors propose, among others, that they reveal the first evidence that wild chimpanzees are able “to combine meaning-bearing units into larger structures” – i.e., that they are capable of semantic compositionality and, by extension, syntax. Their analysis represents an important addition to a growing body of research and discussions on communicational combinatoriality in wild primates and specifically apes, and, by extension, extinct hominins. Incidentally, I have recently published a paper in Animal Cognition in which I also suggested, based on a reanalysis of existing data, that wild chimpanzees can display semantic compositionality and syntax, i.e., are able to combine meaningful units [Gabrić (2021) Anim Cogn, online ahead of print]. In the present commentary, I argue that Leroux et al.’s (2021) interpretation of the data is ungrounded given that (1) unlike for food calls, there is currently very little if any indication in the scientific literature that pant-hoots have semantic content, i.e., are meaningful, (2) Leroux et al. (2021) did not investigate their a priori assumption that the observed pant-hoots are in fact meaningful/semantic, (3) they did not report on recipients’ behaviors in association with neither the individual nor combined calls, and (4) they did not compare the callers’ behaviours in association with the individual calls vs. combined calls. Since pant-hoots feature prominently in the chimpanzee vocal repertoire and the debate on their eventual meaningfulness/semanticity is still wide open, this represents a fine opportunity to revisit this issue in the context of Leroux et al.’s (2021) study. Their paper further raises several other less significant questions. Notwithstanding, their paper brings important novel insights into communicational combinatoriality in wild chimpanzees and supports the notion of using linguistic methods in wild animal communication research.
... For example, it has been shown that linguistic labels can (1) enlarge perceived differences between targets and distractors in visual search (Lupyan, 2008;Lupyan & Spivey, 2010;Lupyan & Swingley, 2018), (2) affect visual motion perception (Dils & Boroditskty, 2010;Francken et al., 2015;Meteyard et al., 2007), (3) affect contrast sensitivity (Pelekanos & Moutoussis, 2012), and (4) affect face perception (Landau et al., 2010). Moreover, the influence of communicative acts (i.e., language) on vision appears not to be limited to the human species, as Suzuki (2018) showed that vision of Japanese tits (Parus minor) is affected by alarm calls of fellow birds: When hearing such calls, Suzuki's birds became more perceptive to objects resembling snakes. Although it is disputed whether the above results actually show that cognition is embodied (see, for example, Firestone & Scholl, 2016), the emerging conclusion is that linguistic labels activate neural structures also involved in actually perceiving the information the labels refer to. ...
Article
Full-text available
One of the most influential ideas within the domain of cognition is that of embodied cognition, in which the experienced world is the result of an interplay between an organism’s physiology, sensorimotor system, and its environment. An aspect of this idea is that linguistic information activates sensory representations automatically. For example, hearing the word ‘red’ would automatically activate sensory representations of this color. But does linguistic information prioritize access to awareness of congruent visual information? Here, we show that linguistic verbal cues accelerate matching visual targets into awareness by using a breaking continuous flash suppression paradigm. In a speeded reaction time task, observers heard spoken color labels (e.g., red) followed by colored targets that were either congruent (red), incongruent (green), or neutral (a neutral noncolor word) with respect to the labels. Importantly, and in contrast to previous studies investigating a similar question, the incidence of congruent trials was not higher than that of incongruent trials. Our results show that RTs were selectively shortened for congruent verbal–visual pairings, and that this shortening occurred over a wide range of cue–target intervals. We suggest that linguistic verbal information preactivates sensory representations, so that hearing the word ‘red’ preactivates (visual) sensory information internally.
Article
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Humans communicate with each other through language, which enables us talk about things beyond time and space. Do non-human animals learn to associate human speech with specific objects in everyday life? We examined whether cats matched familiar cats’ names and faces (Exp.1) and human family members’ names and faces (Exp.2). Cats were presented with a photo of the familiar cat’s face on a laptop monitor after hearing the same cat’s name or another cat’s name called by the subject cat’s owner (Exp.1) or an experimenter (Exp.2). Half of the trials were in a congruent condition where the name and face matched, and half were in an incongruent (mismatch) condition. Results of Exp.1 showed that household cats paid attention to the monitor for longer in the incongruent condition, suggesting an expectancy violation effect; however, café cats did not. In Exp.2, cats living in larger human families were found to look at the monitor for increasingly longer durations in the incongruent condition. Furthermore, this tendency was stronger among cats that had lived with their human family for a longer time, although we could not rule out an effect of age. This study provides evidence that cats link a companion's name and corresponding face without explicit training.
Article
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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 (Hum. Evol. 6:81–89, 1991) 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.
Article
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Human language can express limitless meanings from a finite set of words based on combinatorial rules (i.e., compositional syntax). Although animal vocalizations may be comprised of different basic elements (notes), it remains unknown whether compositional syntax has also evolved in animals. Here we report the first experimental evidence for compositional syntax in a wild animal species, the Japanese great tit (Parus minor). Tits have over ten different notes in their vocal repertoire and use them either solely or in combination with other notes. Experiments reveal that receivers extract different meanings from ‘ABC’ (scan for danger) and ‘D’ notes (approach the caller), and a compound meaning from ‘ABC–D’ combinations. However, receivers rarely scan and approach when note ordering is artificially reversed (‘D–ABC’). Thus, compositional syntax is not unique to human language but may have evolved independently in animals as one of the basic mechanisms of information transmission.
Article
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What do animal signals mean? This is a central question in studies on animal communication. Research into the semantics of animal signals began in 1980, with evidence that alarm calls of a non-human primate designated predators as external referents. These studies have challenged the historical assumption that such referential signaling is a unique feature of human language and produced a paradigm shift in animal communication research. Over the past two decades, an increasing number of field studies have revealed similar complexity in anti-predator communication of birds. The acoustic structures of avian alarm calls show a high degree of variation in pitch, duration, shape, and repetition rate. In addition to such distinct and graded variations, several birds combine discrete types of notes or calls into higher complex sequences. These variations in alarm calls are typically associated with the predator’s attributes, such as predator type and distance, and receivers respond to them with appropriate anti-predator behaviors. Although alarm calls of several bird species, as well as those of monkeys, appear to denote predator attributes, almost nothing is known about the cognitive processes that underlie the production and perception of these signals. In this review, I explore the existing evidence for referential signaling in birds and highlight the importance of the cognitive approach to animal communication research. I hope this review will promote further investigations of alarm-calling behavior in birds and will help enhance our understanding of the ecology and evolution of semantic communication.
Article
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Mental imagery research has weathered both disbelief of the phenomenon and inherent methodological limitations. Here we review recent behavioral, brain imaging, and clinical research that has reshaped our understanding of mental imagery. Research supports the claim that visual mental imagery is a depictive internal representation that functions like a weak form of perception. Brain imaging work has demonstrated that neural representations of mental and perceptual images resemble one another as early as the primary visual cortex (V1). Activity patterns in V1 encode mental images and perceptual images via a common set of low-level depictive visual features. Recent translational and clinical research reveals the pivotal role that imagery plays in many mental disorders and suggests how clinicians can utilize imagery in treatment. Recent research suggests that visual mental imagery functions as if it were a weak form of perception.Evidence suggests overlap between visual imagery and visual working memory - those with strong imagery tend to utilize it for mnemonic performance.Brain imaging work suggests that representations of perceived stimuli and mental images resemble one another as early as V1.Imagery plays a pivotal role in many mental disorders and clinicians can utilize imagery to treat such disorders.
Article
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Parents of many bird species produce alarm calls when they approach and deter a nest predator in order to defend their offspring. Alarm calls have been shown to warn nestlings about predatory threats, but parents also face a similar risk of predation when incubating eggs in their nests. Here, I show that incubating female Japanese great tits, Parus minor, assess predation risk by conspecific alarm calls given outside the nest cavity. Tits produce acoustically discrete alarm calls for different nest predators: "jar" calls for snakes and "chicka" calls for other predators such as crows and martens. Playback experiments revealed that incubating females responded to "jar" calls by leaving their nest, whereas they responded to "chicka" calls by looking out of the nest entrance. Since snakes invade the nest cavity, escaping from the nest helps females avoid snake predation. In contrast, "chicka" calls are used for a variety of predator types, and therefore, looking out of the nest entrance helps females gather information about the type and location of approaching predators. These results show that incubating females derive information about predator type from different types of alarm calls, providing a novel example of functionally referential communication.
Article
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Avian nests face a wide variety of nest predators, which pose different risks that could select for the ability of parents to notify conspecifics of nest predator type. We previously demonstrated that the Japanese Tit (Parus minor) produces acoustically distinct mobbing calls for different nest predators (crows and snakes), thereby eliciting different and appropriate anti-predator responses not only in parents, but also in nestlings. However, the variation in mobbing call behavior may have been caused by differences in the experimental methods used, whereby each nest was presented with either a mounted crow or a live caged snake. In the present study, we observed a total of seven natural encounters of Japanese Tits with crows (n = 4) and snakes (n = 3) near their nests. Consistent with the previous experiments, Japanese Tits produced distinct mobbing calls, namely, "chicka" calls for crows (4/4) and "jar" calls for snakes (3/3). Thus, we conclude that mobbing calls of Japanese Tits signal nest predator type to both parents and nestlings.
Article
Perception can be described as a process of inference, integrating bottom-up sensory inputs and top-down expectations. However, it is unclear how this process is neurally implemented. It has been proposed that expectations lead to prestimulus baseline increases in sensory neurons tuned to the expected stimulus, which in turn, affect the processing of subsequent stimuli. Recent fMRI studies have revealed stimulus-specific patterns of activation in sensory cortex as a result of expectation, but this method lacks the temporal resolution necessary to distinguish pre- from poststimulus processes. Here, we combined human magnetoencephalography (MEG) with multivariate decoding techniques to probe the representational content of neural signals in a time-resolved manner. We observed a representation of expected stimuli in the neural signal shortly before they were presented, showing that expectations indeed induce a preactivation of stimulus templates. The strength of these prestimulus expectation templates correlated with participants' behavioral improvement when the expected feature was task-relevant. These results suggest a mechanism for how predictive perception can be neurally implemented.
Article
The generative power of human language depends on grammatical rules, such as word ordering, that allow us to produce and comprehend even novel combinations of words [1-3]. Several species of birds and mammals produce sequences of calls [4-6], and, like words in human sentences, their order may influence receiver responses [7]. However, it is unknown whether animals use call ordering to extract meaning from truly novel sequences. Here, we use a novel experimental approach to test this in a wild bird species, the Japanese tit (Parus minor). Japanese tits are attracted to mobbing a predator when they hear conspecific alert and recruitment calls ordered as alert-recruitment sequences [7]. They also approach in response to recruitment calls of heterospecific individuals in mixed-species flocks [8, 9]. Using experimental playbacks, we assess their responses to artificial sequences in which their own alert calls are combined into different orderings with heterospecific recruitment calls. We find that Japanese tits respond similarly to mixed-species alert-recruitment call sequences and to their own alert-recruitment sequences. Importantly, however, tits rarely respond to mixed-species sequences in which the call order is reversed. Thus, Japanese tits extract a compound meaning from novel call sequences using an ordering rule. These results demonstrate a new parallel between animal communication systems and human language, opening new avenues for exploring the evolution of ordering rules and compositionality in animal vocal sequences.
Article
Language, more than anything else, is what makes us human. It appears that no communication system of equivalent power exists elsewhere in the animal kingdom. Any normal human child will learn a language based on rather sparse data in the surrounding world, while even the brightest chimpanzee, exposed to the same environment, will not. Why not? How, and why, did language evolve in our species and not in others? Since Darwin's theory of evolution, questions about the origin of language have generated a rapidly-growing scientific literature, stretched across a number of disciplines, much of it directed at specialist audiences. The diversity of perspectives - from linguistics, anthropology, speech science, genetics, neuroscience and evolutionary biology - can be bewildering. Tecumseh Fitch cuts through this vast literature, bringing together its most important insights to explore one of the biggest unsolved puzzles of human history.