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First published online December 1, 2006
Journal of Experimental Biology 209, 4994-5004 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02609
Acoustic communication in territorial butterflyfish: test of the sound production hypothesis
Department of Zoology and Hawaii Institute of Marine Biology, University of Hawaii at Manoa, Honolulu, HI 96822, USA
* Author for correspondence (e-mail: tricas{at}hawaii.edu)
Accepted 19 October 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: butterflyfish, Chaetodon, vocalization, laterophysic, lateral line, hearing, communication
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Chiszar, 1978;
Guthrie and Muntz, 1993).
However, visual displays in fish are often complemented by acoustic stimuli
that can improve information transfer or reduce signal ambiguity. For example,
in some species a sound or mechanical stimulus produced during visual
stimulation by males is necessary to evoke female courtship
(Tavolga, 1956;
Myrberg et al., 1986;
Ladich, 1990;
Lobel, 1992;
Mann and Lobel, 1998), enhance
territory defense (Myrberg,
1997) and spawning (Satou,
1994a; Satou,
1994b). Thus, it is often necessary to understand the stimuli and
functions of multiple sensory systems to interpret the evolution of behavioral
displays and social interactions.
Butterflyfishes (family Chaetodontidae, Perciformes) are diverse (
126
spp), highly social and conspicuous inhabitants of almost all coral reefs
(Allen, 1980;
Findley and Findley, 2001).
Members of this family are diurnal and exhibit numerous forms of complex
social and mating behaviors that include monogamous pairing, haremic mating
systems, solitary behavior and aggregation or schooling
(Reese, 1975;
Hourigan, 1989). Past studies
demonstrate that visual signals in butterflyfishes are important for the
recognition of conspecifics (Zumpe,
1965), location and identification of mates
(Reese, 1975;
Yabuta, 2002), territory
defense (Tricas, 1985;
Tricas, 1989;
Roberts, 1992;
Wrathall et al., 1992;
Kosaki, 1999), threats from
predators (Motta, 1984;
Neudecker, 1989) and
indicators of behavioral state (Hamilton
and Peterman, 1971). These studies on butterflyfish behavior
demonstrate that visual signals provide important information in contexts of
community ecology, social behavior and fitness.
Although vision is clearly involved in butterflyfish communication,
acoustic signals may also be important during behavioral interactions. Members
of the genus Chaetodon have swim bladder horns and a morphological
feature known as the `laterophysic connection' that may be a unique vertebrate
adaptation for processing of acoustic stimuli
(Fig. 1). Bilaterally paired
anterior horns of the swim bladder project rostrally and near a medial opening
of the supracleithrum bone where the head and trunk lateral line systems join
(Blum, 1988;
Webb, 1998). Among the 12
Chaetodon subgenera are several anatomical variations in the length
of swim bladder horns, their association with the supracleithrum lateral line
canal, and intervening soft tissues (Webb
and Smith, 2000; Smith et al.,
2003; Webb et al.,
2006). This unique morphology in Chaetodon has lead to
the proposal that their inner ear and part of the lateral line may be
sensitive to sound pressure. However, the relevant stimuli, receiver
mechanisms and functions for these putative hearing structures were
unknown.
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;
Kalmijn, 1989). In some
species the inner ear is also stimulated by local particle motion that results
from sound pressure induced pulsations of the adjacent air-filled swim bladder
or other gas-filled structures in proximity to the ear
(Coombs and Popper, 1979;
Denton and Gray, 1993;
Yan and Curtsinger, 2000;
Fletcher and Crawford, 2001).
Therefore, in addition to stimulation of the ear by particle velocity fields,
the swim bladder in Chaetodon may transform sound pressure into local
movement of the anterior horns that stimulate the inner ear. Movement of the
swim bladder horns may also displace the adjacent laterophysic tympanum that
in turn creates fluid motion within the lateral line in the supracleithrum
bone (Webb, 1998). This
proposed transduction of sound pressure to the lateral line is novel, but the
response characteristics of the laterophysic system to relevant stimuli remain
to be tested.
One important assumption of acoustic stimulus processing in
Chaetodon is that these accessory structures have evolved to enhance
the reception of relevant sounds such as those produced during natural social
behaviors. Electric shock techniques were used to evoke sounds from several
reef fishes, including short pulses from single Chaetodon in holding
tanks (Fish and Mowbray,
1970). However, to date there are no reports of sound production
by Chaetodon in natural settings despite the many studies on their
well-known and visually mediated social and agonistic behaviors (e.g.
Reese, 1975;
Tricas, 1985;
Tricas, 1989;
Fricke, 1986;
Hourigan, 1989;
Kosaki, 1999;
Lobel, 1989;
Roberts and Ormond, 1992;
Yabuta, 2002). Some possible
explanations to explain the failure to detect and identify sounds in naturally
behaving species are that vocalizations are infrequent, of low intensity,
masked by ambient environmental noise, or not produced by captive fish. Thus,
a test for sound production by butterflyfish in a normal social setting is
necessary to establish the natural acoustic repertoire and sound
characteristics, and provide insight into possible biological functions of the
unique swim bladder and laterophysic morphology.
This study presents an experimental test of the prediction that Chaetodon produces weak sounds during their normal social behavior on coral reefs. We used presentations of conspecific intruders into feeding territories of a monogamous species to evoke aggressive visual territorial displays and acoustic behaviors. In addition, we identify sounds produced among intruder fish pairs, thus sound production occurs in contexts of both extra- and intra-pair communication. These findings emphasize the possible importance of weak acoustic signals for social communication in this group, and are consistent with the proposal that the unique laterophysic/swim bladder morphologies evolved to enhance the auditory capabilities of Chaetodon.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Tricas 1989;
Hourigan, 1989;
Kosaki, 1999). This species is
endemic to the Hawaiian Islands and Johnston Atoll, distributed widely over
coral-rich reefs of Hawaii, and is easily accessed by divers. It is an
obligate corallivore and pairs are known to maintain territories of 50-100
m2 for periods of >4 years. We expected this species to have
enhanced auditory capabilities because it has a well-developed laterophysic
system and prominent swim bladder horns that project near the inner ear
(Webb and Smith, 2000;
Smith et al., 2003;
Webb et al., 2006).
Acoustic recording experiments
Field experiments were conducted at Puako Reef on the west coast of the
island of Hawaii (19.93°N, 155.86°W). This study site has extensive
fields of stony corals (Pocillopora meandrina, Porites lobata and
Porites compressa) that extend from the shallow reef flat seaward to
depths of about 25 m where pairs of C. multicinctus establish
permanent and contiguous feeding territories. Scuba divers identified
experimental pairs that maintained feeding territories at depths of 8-20 m.
Pairs were observed for approximately 15 min to identify the territory
boundary and to confirm the pair association. The experimental pair was then
challenged by the introduction of conspecific intruders placed in a model
bottle, a technique that is known to evoke strong defense behaviors by the
resident pair (Tricas, 1989;
Kosaki, 1999). Intruder fish
were collected each day by hand net >50 m away from the experimental area,
placed either singly or in pairs within a transparent 1-l glass bottle, capped
with a perforated lid for ventilation, and positioned near the center of the
territory. Acoustic and motor behaviors were recorded with a digital video
camera (30 frames s-1, 20-20 000 Hz audio band pass) in an
underwater housing and a hydrophone (FishPhone, BioAcoustics, MA, USA;
frequency response=8-4000 Hz; sensitivity=-148 dBv/µPa ±1.7 dB)
connected to the audio input. This system provided good acoustic recordings
but the automatic gain control precluded analysis of absolute sound pressure
levels. The hydrophone was placed near or fixed to the side of the bottle, and
the camera positioned approximately 1 m away to simultaneously record
behavioral interactions and associated sounds
(Fig. 2). Since we initially
did not know whether sounds would be produced or recordable, we implemented
variable time durations for the initial experimental sessions that lasted from
5-43 min. After the start of a recording session, divers swam >50 m away to
reduce ambient acoustic background noise produced from the open circuit scuba
exhaust. A session was ended when divers returned to the site and moved the
setup to the next test territory. To confirm that behavioral responses and
sounds were directed at conspecific intruders, control recording sessions were
conducted in which the camera, hydrophone and an empty bottle were
placed in fish territories (N=3) for 15 min and the behaviors/sounds
recorded. These control tests revealed that resident pairs made brief
approaches to the introduced bottle, but showed no agonistic behavior or
audible sounds. Thus, the aggressive behavior and acoustic responses observed
in our presentation experiments could be attributed to the presence of
introduced conspecifics.
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Use of animals was approved by the University of Hawaii Institutional Animal Care and Use Committee.
Video tapes were screened for acoustic sounds on a video cassette recorder and monitor in the lab. Each putative acoustic vocalization and any associated locomotor or display behaviors were categorized to identify acoustico-motor behaviors, kinematics, and determine which fish (territory residents or bottled intruders) produced the vocalization. Behavioral sequences were then transferred from tape to a computer and analyzed using Cinestream 3.1 (Autodesk, San Rafael, CA, USA) for the temporal association between motor patterns and sound production. Sound files (raw sample rate=44.1 kHz) were then exported and analyzed with Cool Edit Pro (Syntrillium, Phoenix, AZ, USA) software for temporal and frequency features. Some sounds had strong low frequency content, thus these waveforms were resampled at 4000, 2000 or 200 samples s-1 for analysis of low frequencies. Frequency analyses were performed using fast Fourier transformations (FFT Hanning with either a 128 or 256 sample window) and spectrograms. Aggressive behaviors that produced an audible ring caused by contact with the glass bottle were excluded from acoustic analyses.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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=10.6 min session-1).
Prior to the introduction of conspecific intruders, experimental pairs foraged
widely across their territory, showed normal movement patterns and intra-pair
behaviors and almost no aggressive behaviors with other conspecifics as
demonstrated in previous experiments on this species
(Tricas, 1985;
Tricas, 1989). After placement
of bottled conspecific intruders into a territory, resident pairs quickly
detected, approached, displayed and attacked the introduced fish
[delay=10.0±0.0002 s (
± s.d.; N=15 pairs)]. This aggressive behavior resulted in a
high proportion of the pair's time budget
(=80.0%) spent <1 m from the
model-bottle and thereby simulated natural but prolonged territorial
encounters. Bottled intruders typically were stationary when residents were
out of sight but faced residents when approached.
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) but we did not
capture fish to confirm their sex. Acoustic analyses identified five distinct
sounds that included both single pulses and pulse trains. Most acoustic
behaviors were associated with specific motor patterns.
The tail slap
Territory residents always showed strong aggression that included frontal
approaches, static lateral displays and swimming behavior directly in front of
or around the intruder fish. Escalated aggressive displays were frequently
followed by a strong tail slap delivered at a distance of less than one body
length from bottled fish (Fig.
3A). Frame-by-frame analysis revealed that the tail slap behavior
begins with a lateral display, slow approach, and flexion of the head and
caudal portion of the body away from the intruder. This lateral display
behavior is terminated by a quick tail slap at the intruder followed by a turn
and forward acceleration of the body. The average duration of the tail slap
action pattern was 193 ms (Table
1).
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Two distinct acoustic sounds were recorded during the tail slap behavior
(Fig. 3A,
Fig. 4A). A low frequency pulse
sound was produced in association with motion of the body during the tail slap
and had an average duration of 154 ms
(Table 1). This low frequency
sound had a peak frequency between 51and 109 Hz
(=69 Hz), and was associated with
hydrodynamic flow created by motion of the posterior body that often displaced
suspended particulates in the water column and sometimes the nearby mate.
However, the hydrodynamic pulse was often difficult to record due to the
directionality of the tail slap, the solid wall of the bottle that often
blocked hydrodynamic signals to the hydrophone and the rapid attenuation with
distance.
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=10 ms) and most commonly occurred
during tail flexion associated with the rapid turn behavior
(Table 1,
Fig. 4A). The click was
broadband and of relatively high peak frequency
(=3415 Hz). The tail slap behavior
was sometimes produced sequentially by the male and female pair as they swam
by the bottled fish, thus producing aggressive and complex visual,
hydrodynamic and acoustic signals to the intruders. This acoustic behavior was
the most frequent observed and accounted for almost half of the recorded
sounds (Fig. 5).
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0.5 m
and finally a second turn to start an intense lateral display. The
display is presented during lateral swimming, involves partial erection of the
medial fins, includes a bending of the head away from the bottled intruder,
and presents a clear visual signal to the bottled fish. The jump behavior
(excluding the approach and lateral display) duration ranged from 231-429 ms
(=341 ms).
Acoustic sounds during the jump behavior coincided with either the turn or
the ascend motions. Like the tail slap, a low frequency pulsed movement of
water is produced during the turn behavior
(Fig. 3C,
Fig. 4B). The turn was either
accompanied or followed by a series of rapid acoustic pulses and a subtle
rapid body shake that was not always obvious during upward swimming. The jump
sound was a train of four to eight pulses with an average duration of 301 ms
(Fig. 6,
Table 1). Single pulses were of
short duration (=19 ms), had usually
regular interpulse periods (=54 ms),
and an average pulse peak frequency of 466 Hz. This behavior was relatively
infrequent (Fig. 5) and
observed only in highly aggressive resident fish.
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Pelvic fin flick
Both residents and bottled fish produced sounds associated with extension
of their pelvic fins (Fig. 3C).
The pelvic fin flick motor pattern occurred when residents and intruders faced
each other, was of relatively long duration
(=238 ms) and consisted of a rapid
ventral extension of both pelvic fins (that occurred in less than one video
frame=33 ms) followed by a slower retraction. No other body movements (fin
extensions or body motion) were observed during this behavior. The pelvic fin
flick produced a brief acoustic pulse that occurred before maximum extension
of the fin (Fig. 6A). This
sound was of short duration (=17 ms),
a mean peak frequency of 229 Hz and included 20% of all observed sounds
(Fig. 5). No pulse trains were
observed with this behavior.
The dorsal-anal fin erect
Partial erection of the medial fins is common during lateral displays among
territory residents, primarily involves elevation of the soft caudal portion
of the dorsal and anal fins (rarely the spines), and was not observed to
include the production of sound. In contrast, the dorsal-anal fin erect
behavior included full extension of the dorsal and anal fin spines and was
observed in only one fish during an intense lateral swimming display
(Fig. 5). This behavior was
accompanied by the production of a distinct sound of 115 ms duration and a
peak frequency of 125 Hz (Table
1).
Grunt train
The grunt train sound was produced by bottled fish pairs when confronted by
territory residents. This acoustic behavior often began when the resident pair
approached the bottled intruders (>3 m away), and continued during direct
confrontations and displays by residents
(Fig. 3D). Unlike all other
acoustic behaviors, no clear associated motor movements were observed on
video. Thus, the grunt sound is most likely generated by internal muscles that
do not influence movement of the fins or body. Although it is possible that
free-swimming resident fish could also produce this sound, we have several
reasons to conclude that our recorded grunt trains were from bottled intruder
fish. First, this grunt sound often began when approaching residents were
visible but at large distances from the intruder. Next, we would expect sound
amplitude to be relatively constant if produced by bottled fish and variable
if produced by the wide-moving territory residents. Our recordings show that
the amplitude of grunt pulses, which were detected by the hydrophone that was
fixed to the side of the bottle, did not change as free-swimming residents
approached, swam in the vicinity, or swam away. Finally, the pulse trains were
not interrupted when resident fish produced other acoustic behaviors.
The grunt acoustic behavior was recorded primarily when bottled fish were
presented in pairs, and rarely from a single bottled fish. The grunt train was
the most common sound produced by bottled intruders
(Fig. 5) and consisted of a
sequence of individual pulses produced at a rate of about 3 pulses
s-1 that lasted for an average duration of 5.7 s
(Fig. 6B,
Table 1). We were unable to
distinguish which of the two bottled fish produced the grunt train, but in
most cases pulses were of constant amplitude and uniform period, which
indicate a grunt train was most likely produced by a single individual.
However, in a few records inter-pulse intervals were irregular and thus are
probably the result of simultaneous grunts trains produced by both bottled
fish. With the exception of the low frequency hydrodynamic pulses produced by
territorial fish during the tail slap, single grunt pulses were of the longest
duration (=42 ms), had a mean peak
fundamental frequency of 163 Hz and were of low bandwidth. Several harmonics
were often associated with this sound.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Acoustic behavior in Chaetodon
This study revealed the production of five sounds that are associated with
agonistic visual displays during interactions between territory residents and
bottled intruders. The most frequent acoustic behavior was the tail slap made
by territory residents and directed towards intruder fish. This behavior was
always preceded by a lateral display, a common form of aggression during
initial border disputes among territory holders in this and other species
Chaetodon spp. (Zumpe,
1965; Sutton,
1985; Yabuta,
2002), and in cichlids is an initial signal of low intensity
(Baerends and Baerends-van Roon,
1950; Enquist and Leimar,
1983). In escalated encounters by territory resident
Chaetodon, the lateral display could be followed by the dorsal-anal
fin extension behavior or the tail slap behavior at a distance of one to two
body lengths from the receiver. The use of relatively weak tail slaps or
`beating' during lateral displays is common in fishes (Chizar, 1978), and is
described for some cichlids as stationary swimming with strong undulations
(Barlow, 1967), and a
low-intensity aggressive behavior (Enquist
and Lemar, 1983; Brick,
1998). By contrast, the tail slap behavior by C.
multicinctus is brief but probably energetically expensive. It is very
rapid and intense, usually follows several low-level agonistic lateral
displays and occurs at the end of a single bout. The motion of the body during
the tail slap produces a strong hydrodynamic pulse with a peak frequency
<100 Hz (down to and probably below the 20 Hz limit of our recording
system). This transient, low-frequency hydrodynamic stimulus is directed at
and can displace the target fish. Low frequency hydrodynamic stimuli were
reported up to 100 Hz for startle response
(Bleckmann et al., 1991) and up
to 300 Hz for rapid swimming (Gray and
Denton, 1991) behaviors. Since the force that produces water
displacement by Chaetodon is likely a function of body size, the
hydrodynamic flow from the tail slap together with visual stimulation from the
lateral display may provide an integrated honest signal of size or status
during territorial challenges as described for tail beating during nesting in
the Siamese fighting fish (Halperin et al., 1995).
The late phase of the tail slap behavior in C. multicinctus
includes a brief acoustic click with a duration of 10 ms, high peak average
frequency of 3.6 kHz of high bandwidth that extends up to more than 15 kHz
(Fig. 3A), and a peak intensity
of 120 dB re. 1 µPa at a distance of <10 cm from the source (T.C.T.
and K. Boyle, unpublished data). The click is within the band of ambient reef
noise produced by snapping shrimp which is of much shorter duration (10 µs)
but much higher intensity 180 dB re: 1 µPa
(Au and Banks, 1998). The
production of high frequency broadband clicks during agonistic interactions
with conspecifics was also reported in other fishes
(Caldwell and Caldwell, 1967;
Valinsky and Rigley, 1981;
Crawford et al., 1997).
However, the question of whether this high frequency sound is perceived by
butterflyfish or serves some other function such as predator deterrence
(Vester et al., 2004) remains
to be tested.
The jump was a rare but strong aggressive behavior that involved clear
visual and pulsed acoustic displays. Single and train pulsed sounds are a
common form of aggressive and courtship behaviors in other coral reef species,
and are best studied in the damselfishes
(Myrberg, 1972;
Myrberg et al., 1986;
Lobel and Mann, 1995). The
humbug damselfish (Dascyllus albisella) and the bicolor damselfish
(Stegastes partitus) produce several different pulsed sounds that are
related to aggression, courtship and visiting and can be distinguished by
pulse duration, period and number
(Myrberg, 1972;
Kenyon, 1994;
Mann and Lobel, 1998).
Although such sounds may be associated with specific behavior contexts,
Myrberg provided experimental evidence that the chirp sound produced by male
bicolor damselfish serves as a territorial `keep out' display, and was most
effective when paired with the visual presence of a resident fish
(Myrberg, 1997). Unlike the
variety of pulsed sounds produced by damselfishes that may serve as
advertisement for defense of a relatively small territory, the aggressive
pulsed sounds in Chaetodon were only observed during the jump
behavior directed toward bottled fish. Since paired butterflyfishes constantly
move about a large feeding territory
(Tricas, 1989), this acoustic
behavior probably occurs primarily during border disputes and escalated
attacks among territory pairs.
The pelvic fin flick behavior was produced by both territory residents and
intruders. This behavior occurred when fish were in a face-to-face
orientation, produced a coincident visual stimulus created by the
ventrolateral extension of the white fins and a short sound pulse, and
potentially may function as a mild agonistic display. Pelvic fin `flickering'
in cichlid fishes is not considered to be a socially relevant behavior
(Baerends and Baerends-van Roon,
1950; Ostrander and Ward, 1995), thus this needs further
investigation in butterflyfish.
The grunt train acoustic behavior was recorded only from bottled fish pairs
when territory residents were present or approaching (up to 3 m away), during
aggressive attacks, and for a brief time after departure of the resident pair.
This vocalization, which unlike all other sounds did not include detectable
kinematics, may function as an alert or stress call among monogamous mates.
Loud stress sounds were reported for other fishes when they are handled or
prodded but biological functions for most of these stress calls need testing
(Myrberg, 1981; Smith, 1992).
Although our experimental setup could not monitor vocalizations of resident
pairs away from the bottle, it is possible that intra-pair grunt trains could
be made to alert a free-swimming mate of threats from predators, conspecific
intruders or other competitors.
Fishes show a diversity of morphological adaptations for the production of
sound stimuli that include direct vibration of the swim bladder, stridulation
of bones or teeth, vibration of body parts, and strumming of specialized
tendons (Fine et al., 1977;
Myrberg, 1981;
Hawkins, 1993;
Ladich, 2004). In their survey
of sounds of western north Atlantic fishes, Fish and Mowbray
(Fish and Mowbray, 1970) used
electric shocks to evoke sounds described as small thumps, knocks and toothy
clicks from C. striatus and C. ocellatus isolated in test
tanks. That study reported acoustic frequency components of between 100 and
400 Hz and that the swim bladder was the sonic mechanism. However, although
sounds may be propagated by resonance of the swim bladder, they must originate
from movement of an accessory structure since the swim bladder of
Chaetodon has no extrinsic or intrinsic muscles
(Webb, 1998;
Webb et al., 2006). Although
we could not resolve the mechanism of sound production, our kinematic analyses
demonstrate their association with distinct motor patterns. In the tail slap
behavior, gross movement of the body produces a strong pulse of hydrodynamic
flow that is followed by an acoustic click. The high frequency broadband
characteristics of the click and its association with flexion of the caudal
peduncle indicates possible stridulation
(Katz, 2002), although we
cannot rule out cavitation as occurs in snapping shrimp
(Versluis et al., 2000). The
sound produced by the pelvic fin flick indicates movement of some internal
mechanism linked with structures of the pelvic girdle. Likewise, the sound
created during dorsal-anal fin extension was of low frequency and bandwidth,
indicating it may not result from stridulation. By contrast, the pulse trains
produced during the jump behavior were sometimes associated with slight
quivers of the body whereas the grunt train sound had no obvious associated
motor patterns. Thus these pulse train sounds are likely generated by
movements of internal structures. Further, these latter pulsed sounds showed
strong harmonics that indicate movement of internal body parts that vibrate
the swim bladder (see Hawkins,
1993).
Acoustico-lateralis stimuli in Chaetodon behavior
Biological sources of sound in water produce two distinct physical stimuli
that can stimulate the inner ear and lateral line (reviewed by
Kalmijn, 1989). Physical
motion at the source-water interface produces an incompressible flow of water
commonly of a dipole form. In addition, a sound pressure wave is created that
expands outward from the source. The lateral line of teleost fish is sensitive
to the velocity and acceleration of water across the surface of the skin
(Coombs et al., 1992;
Kroese and Schellart, 1992).
The fish inner ear is primarily sensitive to the particle velocity fields that
accelerate the body and displace the otoliths within it (reviewed by
Kalmijn, 1988;
Kalmijn, 1989;
Schellart and Popper, 1992).
In some species secondary particle displacements in the region of the inner
ear result from sound pressure-induced pulsations of an adjacent air-filled
swim bladder or other gas-filled structures
(Denton and Gray, 1993;
Yan and Curtsinger, 2000;
Fletcher and Crawford, 2001).
Such `otophysic connections' can enhance auditory sensitivity and frequency
response of the ear (Coombs and Popper,
1979), may increase the distance over which acoustic stimuli can
be detected, but provide no directional information (for a review, see
Coombs and Montgomery, 1999).
The genus Chaetodon is distinguished by the presence of bilaterally
paired diverticulae (horns) of the swim bladder that project in close
proximity to the medial surface of the supracleithrum lateral line, and also
approach the inner ear (Blum,
1988; Smith et al.,
2003) which has well-developed sensory maculae
(Popper, 1983). The long swim
bladder horns of Chaetodon multicinctus (subgenus Exornator)
project near to the caudal otic capsule and are separated from the
supracleithrum lateral line by a layer of muscle (indirect laterophysic
connection, Ind2, as per Webb et al.,
2006). Therefore, the inner ear of Chaetodon multicinctus
should be sensitive to hydrodynamic velocity flow fields and sound pressure
via local displacements of the anterior swim bladder horn, whereas
the lateral line is sensitive to hydrodynamic flow across the skin and
possibly sound pressure at the level of the laterophysic connection.
Almost all acoustic behaviors recorded in this study were produced within
one or two body lengths of the receiver fish and may provide several
combinations of multimodal stimuli to the auditory, lateral line and
laterophysic systems in addition to strong visual signals. Strong hydrodynamic
flow fields produced by body motions of the tail slap (and possibly jump)
behavior can displace the receiver's body, stimulate the otolith maculae of
the inner ear and provide intensity and directional information about the
source. Such low frequency sound may provide important auditory stimuli
(Gray and Denton, 1991;
Sand and Karlson, 2000) and
deserves further consideration in this system. In addition, hydrodynamic flow
can differentially stimulate the receiver's ipsilateral lateral line that is
known to provide important cues for fish when close to the source. Sounds that
have peak frequencies between 100 and 500 Hz (e.g. pelvic fin flick, grunt
train, pulse train component of the jump and dorsal-anal fin erection
behaviors) may also stimulate the inner ear, which in many species has high
sensitivity to particle velocity stimulation in this frequency range (reviewed
by Schellart and Popper,
1992). Near field acoustic signals may stimulate both the inner
ear and lateral line in a distancedependent manner to provide directional cues
for the source (Coombs and Montgomery,
1999). Such octavolateralis directional information may be
important during agonistic interactions among individuals of two or more
pairs. In addition, acoustico-lateralis stimuli and communication may be
important for butterflyfish reproduction since C. multicinctus pairs
exhibit body quivers during spawning and a related pomacanthid angelfish
produces various sounds (`clicks' and `grunts') during courtship
(Lobel, 1978).
In addition to direct stimulation of the inner ear in Chaetodon
during social behavior, sound pressure stimuli may induce oscillations of the
swim bladder horns (Webb et al.,
2006). This transduction of sound pressure to particle motion may
produce fluid flow in the supracleithral lateral line or motion of the inner
ear. Acoustic pressure stimuli are converted to fluid motion in the lateral
line of clupeid fishes by the recessus lateralis in which the anterior lateral
line has connections with auditory gas-filled bullae of the inner ear
(Blaxter et al., 1981). Sound
pressure stimuli from putative acoustic signals in Chaetodon may
indeed stimulate motion of the swim bladder horns and adjacent segments of the
head lateral line, but the physics of function and any biological importance
remain to be demonstrated.
In conclusion, we have shown that a territorial monogamous butterflyfish in
its natural habitat reef produces several sounds during visual agonistic
interactions with conspecific competitors and mates. This finding is
consistent with the hypothesis that sound is important for social
communication in Chaetodon. Although Chaetodon multicinctus
produces sounds, the question of whether they provide an adaptive advantage to
the sender, receiver or both (sensu
Myrberg, 1981) now requires
experimental confirmation. One possible result of the production of weak
sounds by these fish may be the requirement of close associative behaviors for
acoustic reception such as pairing and group behaviors that are widespread in
Chaetodon (Hourigan,
1989; Roberts and Ormond,
1992). Future work is needed to quantitatively characterize the
frequency spectra and intensity of sounds produced by Chaetodon,
determine butterflyfish hearing thresholds and bandwidths, and test whether
the laterophysic connection and swim bladder horns enhance hearing
capabilities of sounds produced during social interactions. In addition,
quantitative measurements of near field particle motion and sound pressures
produced by behaviors during their natural interactions are required to
determine the relative importance of each stimulus.
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Acknowledgments |
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Footnotes |
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Present address: Department of Biology, Florida Atlantic University, Boca
Raton, FL 33431, USA 
Present address: NOAA, Northwestern Hawaiian Islands Coral Reef Ecosystem
Reserve, 6600 Kalaniana'ole Hwy, Honolulu, HI 96825, USA
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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