ISSN 00329452, Journal of Ichthyology, 2009, Vol. 49, No. 11, pp. 963–1020. © Pleiades Publishing, Ltd., 2009.

Acoustic Signaling in Fish

A. O. Kasumyan
Moscow State University, Moscow, 119899 Russia;
email: alex.kasumyan@mail.ru
Received June 24, 2009

Abstract—The paper lists basic data on the role of sounds in fish behavior. The involvement of acoustic sig
naling in the control of reproductive, territorial, agonistic, aggressive, social, and feeding behavior in fish that
differ in the systematics and mode of life is considered. Species and population specifics and individual sound
variation in fish, diurnal and seasonal cyclicity of sound activity, and behavior that accompany acoustic sig
naling and the effects upon it of different environmental factors are considered. Evidence on the formation
of acoustic signaling in ontogenesis of fish is provided; the range of sound signaling and correspondence
between sound spectra and auditory sensitivity are discussed. Possible applied aspects of results of study of fish
bioacoustics are analyzed.
DOI: 10.1134/S0032945209110010
Key words: fish, sounds, acoustic signaling, bioacoustics, behavior, ontogenesis, species and population spe
cifics, diurnal and seasonal rhythms.

The sphere of zoology that studies the acoustic ori
entation of animals and their ability to perceive or
exchange with sound signals is called bioacoustics.
Since the acoustic properties of the aquatic and air
environments considerably differ, acoustic signaling in
fish and other aquatic animals, invertebrates and ver
tebrates, are often united by the term biohydroacous
tics. In modern ichthyology, fish bioacoustics has a
comparatively short history, despite the fact that great
ancient philosophers, such as Aristotle (384–322 b.c.)
and Pliny the Elder (23–79 a.d), recorded the ability
1 munication and orientation of fish, on methods of
of fish to generate sounds, and the great inventor and
painter Leonardo da Vinci (1452–1519) suggested to
listen to fish by putting an ear to the oar descended
into water. However, for many centuries, not only
sound generation, but even the presence of auditory
sensitivity in fish was generally negated. Views of this
problem changed fundamentally only at the beginning
of the 20th century when, as a result of special studies,
the presence in fish of a well developed auditory recep
tion was demonstrated. The basic role in this was
played by the studies of the outstanding German
researcher Karl von Fripp (1886–1982). In subse
quent years, especially beginning from the second half
of the 20th century, a large file of experimental data
and numerous results of nature observations were
obtained that convincingly supported the presence in
1
Aristotle in his treatise Historia Animalium mentions several fish
species that emit sounds, and provides a brief characteristic of
these sounds. Later, based on the fish description listed by Aris
totle, the German researcher I. Müller suggested that Aristotle
in his treatise most likely mentions one of species of Sciaenidae,
two representatives of Triglidae, Dactylopterus volitans and Zeus
faber, and probably Misgurnus fossilis (Zograf, 1890).
fish of well developed auditory abilities and diverse
methods of sound generation and the use by them of
acoustic signals in interspecies interactions. A notice
able progress during the last years in the elaboration of
new more advanced technical devices for recording
and analyzing underwater sounds has considerably
extended our knowledge of the acoustical repertoire of
fish and regulation, using sounds, of many most
important forms of behavior.
The purpose of this paper is the analysis and sys
tematization of available data on the acoustical com
exchange between fish with biologically valuable
information present in the sounds they generate, and
on the diversity of forms of fish behavior regulated via
sounds. This paper, which continues the series of
review publications of the author on mechanosensory
systems in fish (Kasumyan, 2003, 2004, 2005, 2008),
focuses on data obtained in the sphere of acoustic sig
naling in fish during the last years. Earlier data were
rather comprehensively considered by the Russian
researcher Protasov (1927–1991) in his book Fish Bio
acoustics that was published in 1965 and is the first
monograph in the world dedicated to sounds emitted
by fish.
THE ROLE OF SOUNDS IN FISH BEHAVIOR
Fish emit sounds in diverse situations in connec
tion with the manifestation of diverse forms of behav
ior—at agonistic interactions and at aggressive con
tacts, during courtship behavior and during spawning,
in the case of a threat of predator’s attack, in fright,
and during feeding. Sounds arise during swimming

963
964 KASUMYAN
also. In most cases, fish emit sounds deliberately, i.e.,
in connection with a certain behavior or in certain sit
uations. Such sounds namely that are called special
ized sounds are used by them for communication pur
poses, as a rule, for regulation of intraspecies relations.
The signal function of most fish sounds became evi
dent for researchers as early as at the very beginning of
special studies in the sphere of underwater bioacous
tics. Subsequently, the correctness of this conclusion
was supported by numerous examples that indicate
that the acoustic activity either precedes the manifes
tation by fish of some behavioral responses or such
response is accompanied by specialized sounds or
sound generation is used for signaling, for instance, for
warning about danger or food presence. In some fish,
2 and proper spawning. Spawning sounds of fish belong
emitting of specialized sounds can be an obligatory
element of their complex behavioral repertoires. An
artificially evoked loss of ability in fish for sound gen
eration in such cases leads to blocking of a certain
behavior or makes it detrimental and does not allow
fish to realize to a full measure some life function, for
instance, protection of their own sites, competition for
a female and attracting it to the nest, spawning, etc.
As compared to other kinds of communication, the
transmission of information, using sound signals, has
several doubtless advantages, such as a high velocity of
distribution and a large distance of action. Thanks to a
directed (directional) auditory sensitivity, fish are able
to determine the location of the signal source, which
makes acoustical communication efficient. Its consid
erable limitations include a complex acoustical back
ground and a repeated reflection of acoustic signals in
most biotopes, first of all, in coastal ones where most
of approximately 1000 fish species that, according to
available data, are capable of sound generation dwell.
Because of a small depth in coastal areas of seas and
oceans, as well as in many shallow water bodies,
sounds emitted by fish have a limited zone of distribu
tion. Therefore, under such conditions, auditory
reception that provides the possibility of fish commu
nication using sounds can be considered as a sensory
system for a small distance. Quite obvious conditions
for acoustical communication are formed in the sea
pelagial and at large depths. However, evidence of how
fish that dwell here realize these possibilities is
extremely scarce and allows, so far, more likely only to
assume rather than to state that deepwater fish or fish
of the open oceanic pelagial actually widely use sounds
for communication.
Reproductive Isolation
Sound generation during reproduction is a typical
specific feature of the biology of most fish capable of
2 Specialized
sounds are generated by fish deliberately in connec
tion with a certain behavior or in certain situations. Such sounds
are generated by organs or structures intended for it (Kasumyan,
2008).
JOURNAL OF ICHTHYOLOGY
sound generation (Fine et al., 1977; Lobel, 1992; Myr
berg and Lugli, 2006). Many fish that emit sounds
vocalize namely during spawning, in other periods of
the life cycle, fish either do not generate sounds or do
it extremely rarely. A close relationship is observed
between the acoustical activity of such fish and the
dates and sites of their spawning. Sound emission can
be related to different phases of the reproduction
period—from early prespawning contacts between
individuals of opposite sexes, when fish males form
aggregations or disperse over individual spawning
sites, manifest aggressiveness towards competitors for
the territory or a female up to later phases that directly
precede spawning, such as attraction of a female by
male and courtship display, stimulation for spawning,
to the category of specialized sounds; according to the
mechanism of generation, they most frequently can be
3
either drumming or stridulating.
The most complex reproductive behavior and the
related auditory communication are developed in ter
ritorial fish or in fish that pass to a territorial mode of
life temporarily with the onset of the reproduction sea
son. Such fish usually alternate sounds addressed to
females and regulating spawning behavior with sounds
that are intended for neighbors of the territory or to
accidentally approaching fish of other species. The
latter type of sounds are related to the regulation of
agonistic relationships or direct aggressive manifesta
tions and will be considered below. Spawning sounds
are also typical for fish in which the territorial behavior
is either manifested indistinctly or is not displayed
altogether.
Spawning sounds in territorial fish that do not
migrate to sites of fish reproduction. Resident fish that
do not perform considerable movements and spend
most time within their own sites and use sounds for
signaling during reproduction include small fish of
coral reefs from the family Pomacentridae. Some of
them live in small colonies. In such colonies, every
male has a site of its own that it protects from other fish
and where it tries to attract a female for spawning. To
attract females that are ready for spawning to its terri
tory, male fish of the genus Pomacentrus (=Stegastes),
Hawaiian dascyllus Dascyllus albisella, blackspot ser
geant Abudefduf sordidus, and blue damselfish Chromis
chromis perform rapid upward migrations to the water
column and equally rapid downward migrations—the
so called signal jumps and dips, whose demonstration
is accompanied by sound emission. The signal impor
tance of jumps and dips is emphasized by the fact that
they are performed with an amazing frequency. Males
3 Drumming
sounds are generated due to rapid contractions of
specialized tympanic muscles that are fixed in most fish by one
or both ends to the walls of the swimming bladder. Stridulating
sounds arise during rubbing of teeth or cranial bones, jaw and
gill apparatuses, fin rays, and vertebrae against each other
(Kasumyan, 2008).
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH 965

of D. abdisella, for instance, perform up to 3000 signal

jumps during a day. It is assumed (Gronell, 1989;
Knapp and Kovach, 1991) that such jumps can serve
also as a specific indicator of the readiness of a male
for spawning and be used by females in choosing a (a)
partner for spawning. During jumps, the velocity of these
small fish (body length does not exceed 10–13 cm) aver
ages 80 cm/s (maximum, 120 cm/s), the time of the
jump of 0.425 s, and the average distance covered of
approximately 34 cm (Mann and Lobel, 1997). A male
from the colony, which first noticed a female that
approached, increases the frequency of signal jumps
and dips. Its actions stimulate a similar behavior also
in adjacent males that compete with it. Performing
jumps and dips, male Hawaiian dascyllus emits a typ
ical sound that resembles chirps. This sound repre (b)
sents a small series, on average, of 5–6 pulses, each of
which lasts approximately 13 ms; the interpulse inter
val is 38 ms; and the sound frequency is approximately
370 Hz. Sound generation takes place throughout
most part of time spent by a male on the jump and dip
(approximately 60%); sound parameters (sound fre
quency and its duration, number of pulses, and the
time of interpulse interval) do not depend either on the
fish velocity or the jump length. Acoustical character
istics of sounds of different Pomacentridae that often
inhabit the same sites of the coral reef differ (Myrberg,
1972; Myrberg et al., 1978; Spanier, 1979; Lobel and
Mann, 1995; Mann and Lobel, 1997, 1998; Lobel,
1999; Picciulin et al., 2002). Fig. 1. Spawning behavior of males of bicolor damselfish
Pomocentrus partitus: (a) tilts to the side and (b) dips (Myr
In Pomacentridae, the spawning behavior and the berg and Spires, 1972).
related sound generation have been comprehensively
studied in several species, in particular, in bicolor
damselfish Pomacentrus (=Eupomacentrus) partitus. In provide communication between a male and a female
colonies of P. partitus, which consist of several individ when they are near each other (Mann and Lobel,
uals of opposite sexes and age, sounds (chirps) are 1998). Males of green damselfish A. abdominalis gen
recorded, on average, up to 20–25 times a minute. erate typical sounds during nest preparation—clean
Males emit them during dips—a rapid downward ing of a small substrate site at their territory. These
migration vertically from an altitude of 0.5–1.0 m. sounds consist of successive acoustical pulses with a
After several dips and jumps, a male bicolor damself duration of 55 ms, each of which arises a when fish
ish, before again rapidly moving downwards, swims a bites off the ground surface. Interpulse intervals in
small distance along the horizontal, tilting to the side these sounds are rather long, more than 200 ms and a
by 20°–45° either to the right or to the left (Fig. 1). sound frequency of 280 Hz. The male drives out fish
Such tilts are the beginning of courtship behavior that entered the territory or approached the nest, irre
towards a female. After lateral tilts and the subsequent spective of their species status. During pursuit, it emits
dip, a male that has attracted a female to its territory, sounds of aggression. To attract a female or to signal
tilting head down and spreading pectoral fins, rapidly neighbors that the territory is occupied, A. abdominalis
swims up to a female and sometimes, slightly nudging do not perform signal jumps. To attract a female that
it and performing rapid sliding dips over the bottom, has approached, a male that usually stays in front of
leads a female to the nest (Myrberg and Spires, 1972). the nest, begins to actively swim along the loop
A female D. albisella that has responded to the male shaped or zigzagshaped trajectories, trying to trap a
courtship and the male that accompanies it swim to female (Fig. 2). If a female responds to courtships and
the nest and move several times above it. Spawning follows it the male begins to emit long sounds, with an
occurs only after several such movements are per average duration of approximately 2 s and representing
formed. Both during preliminary movements above a series of 3–26 pulses of two different types, with a
the nest and during spawning, a male generates sounds frequency of 120–130 Hz and harmonics up to
shorter than chirps that consist, on average, of 2– 1000 Hz. The male also continues to emit such sounds
3 pulses. If signal jumps and the corresponding sounds later when it stays in the nest together with a female.
provide distant signaling, shorter prespawning sounds The loudness of these sounds is such that they can be

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

966 KASUMYAN
(a)
–
(b) – sounds that resemble grunts. Males of the second type
(c)
–
Fig. 2. Spawning behavior of green damselfish Abudefduf
abdominalis (Pomacentridae) accompanied by vocaliza
tion: (a) cleaning by a male of a small site at its territory,
(b) attack and pursuit of individuals of its own species or
fish of other species (Labridae, Chaetodontidae, Scaridae,
Acanthuridae, etc.) that have approached the nest, and
(c) attraction of a female to the nest by energetic swim
ming of a male along loopshaped or zigzagshaped trajec
tories and attempts to trap a female after it. A male emits
elongated sounds if a female responds to its courtship and
follows it. The male continues to emit the same sounds also
later when it is in the nest together with a female. The out
line of the male made by a dotted line denotes the initial
position of the fish and that made by solid line denotes the
terminating position. The figure shows oscillograms of
sounds, the horizontal line length corresponds to 100 ms
(Maruska et al., 2007).
perceived by a female at a distance of 1–2 body length
(Maruska et al., 2007).
The representatives of another well studied fish
group—Gobiidae, also belong to territorial fish. Most
of these smallsized fish that inhabit sea coastal waters
or small rivers lead a solitary mode of life near shelters
at their own sites and do not perform distant move
ments. Unlike Pomacentridae, it is not typical of
Gobiidae to form colonies. Sounds in Gobiidae, as
well as the behavior, related to sound generation, have
been well studied; however, the mechanism of sound
generation has so far not been studied. In the spawning
period in Gobiidae, for a rare exception, only males
vocalize; they are represented by two different forms or
morphoforms—large males of the first type and
smaller males of the second type. Usually males of all
morphotypes participate in spawning, but they differ
in behavior and the use of sounds for signaling.
JOURNAL OF ICHTHYOLOGY
In grass goby Zosterisessor ophiocephalus, which
dwells among thickets of marine algae in the offshore
of the Black and Mediterranean seas, males of the first
type are not only larger, but are also distinguished by
elongated rays in the second dorsal fin (Mazzoldi
et al., 2000; Torricelli et al., 2000). Males of the first
type in Z. ophiocephalus, with the onset of the repro
duction season, construct shelter nests usually as a
burrow in the ground and for attracting a female emit
are also capable of generating the same sounds, but do
not construct nests; females generate no sounds. At
the moment of emission, males draw aside operculi
and slightly quiver with the head. Sounds of males of
the first and second types have similar duration
(approximately 300 ms) and a close number of pulses
that follow in series with equal frequency. However, in
males of the first type, sounds are lower in frequency
and higher in amplitude than in males of the second
type (Malavasi et al., 2003). This agrees well with the
dependence of the sound frequency and amplitude on
the body sizes of an individual common for fish (Myr
berg et al., 1993; Lobel and Mann, 1995; Loesser
et al., 1997; Henglmüller and Ladich, 1999;
Kasumyan, 2008). In the experiment, in the absence
of male of the first type, males of the second type
occupy its shelter, display courtship behavior, and emit
sounds for female attraction, i.e., manifest a behavior
allyacoustic stereotype to a full measure (Malavasi
et al., 2003). This differentiates grass goby from plain
fin midshipman Porichthys notatus (see below).
Males of Padogobius martensii and P. nigricans
begin to emit sounds when a female, having
approached close to the nest, freezes for a while near
the entrance in the immediate vicinity of a male
present in the nest. Males of these gobies continue to
emit sounds outside the nest also when they leave it for
courtship of the approaching female. In male P. mar
tensii, the sound repertoire is more diverse and
includes three different sounds; however, only one of
them, tonal, is emitted outside the nest, with a rela
tively low frequency, 5–8 times a minute. After the
male returns to the nest, sounds are emitted more fre
quently (15–20 times a minute), and they are gener
ated with still greater frequency when a female that
followed the male hesitantly stops before the entrance
to the nest (30–40 sounds per minute). At such
moment, males produce also additional noises that
stimulate a female—rapid and frequent blows by the
head and pectoral fins upon the substrate. With the
female appearance in the nest, the tonal sound
becomes increasingly more rare and gradually disap
pears, but almost immediately the male begins to gen
erate two new sounds: an integrated sound that con
sists of several drums that pass into a long tonal com
ponent and a sound that resembles long drums. The
rate of sound generation increases and reaches maxi
mum towards the moment of spawning by the female
of the first eggs, and then rapidly decreases (Fig. 3).
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
Spawning usually continues for several tens of minutes
or even for more than an hour. During spawning of
eggs, the female turns its abdomen up and adheres to
the nest vault egg after egg. Until the female stays in a
usual position, the rate of sound generation is retained
as high. However, as soon as the female turns abdomen
upward and begins to spawn eggs, sound generation is
gradually retarded. During insemination, when the
male turns abdomen upward, it can become silent for
several minutes. After the termination of the spawn
ing, the female for some time remains motionless,
then it assumes a normal position and leaves the nest
(Lugli et al., 1996).
In males of P. nigricans, sound repertoire consists
of only one sound and its duration averages 330 ms;
the frequency is 60–100 Hz and the average number of
pulses in the sound is 26. As in P. martensii, a female
approach to the nest causes a drastic increase in the
rate of sound production, from 40–80 to 90 times a
minute. If a female, for some cause, leaves the nest,
vocalization continues for several minutes (Lugli et al.,
1996). The painted grass goby Pomatoschistus pictus
has two sounds in its spawning repertoire: short low
frequency thumplike sounds and more prolonged and
highfrequency drumming sounds. Thumplike
sounds with a duration of approximately 80 ms and a
frequency lower than 100 Hz are emitted by the male
goby most frequently, when it is alone in the nest or
accompanies a female to the nest. Drumming sounds
with a duration of hundreds of milliseconds and a fre
quency of approximately 300 Hz are recorded consid
erably less frequently when the male outside the nest,
having spread out fins, stays immovably near the
female (Amorim and Neves, 2007). Other goby species
(Knipowitschia punctatissima, microgobius K. paniz
zae, P. minutus, tubenosed goby P. marmoratus, and
P. canestrini) never emit sounds outside the nest even
if they notice a female and begin to display an interest
in it. Sound emission in them begins only after a
female enters the nest, and, on the whole, has the same
dynamics as in other gobies. Gobies of the studied spe
cies whose lifetime is approximately one year have
small sizes, and their body length rarely exceeds
10 cm. It is possible to record sounds only in the
immediate vicinity of fish, and already several centi
meters from it, the sound pressure level becomes very
low, apparently, lower than the threshold. In this con
nection, there is a point of view according to which
sounds emitted by males of these goby species within
the nest serve not for female stimulation but are used
by the male to signal that it is prepared to begin spawn
ing and of its reproductive potential. This suggestion is
evidenced not only by the small sizes of the acoustic
field formed by males whose boundaries are unlikely to
extend beyond the nest limits, but also by a drastically
increasing sound activity of males during female pres
ence in the nest, as well as by frequently observed cases
when a female leaves the nest before the beginning of
spawning (Lindström, 1992; Lugli et al., 1997; Lugli
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
967
Number of sounds per minute
15
10
5
10 20 30 40 50 60 70 80 90
Time, min
Fig. 3. Sound activity (number of sounds per minute) of two
males of Padogobius martensii during successive 5min inter
vals from the moment of the start of spawning (deposition
by a female of the first eggs) and up to its termination
(departure of a female from the nest). The sound activity of
two different males is designated by solid and dotted lines
(Lugli et al., 1997).
and Torricelli, 1999; Lindström and Lugli, 2000). It is
assumed that a rapid assessment of the male potential
is a typical feature of behavior of female gobies in
choosing a nuptial partner (Forsgren, 1997). For
attracting females to the nest, male round goby Neogo
bius melanostomus emits sounds. These sounds that
resemble croaking or squeaks attract females that
gather around the nest. The male selects one of them,
lashes its tail near it, and tries to lead it to the nest. It is
of interest that a female ready for spawning not only
assumes a certain posture (fins pressed to the body,
raised head), but also emits weak sharp squeaks. A
strong attractive effect on females is also made by the
playback of recordings of male sounds at sites of natu
ral spawning of these fish (Protasov et al., 1965). For
proper males, the sounds emitted by adjacent males
are lowefficient stimuli and almost do not affect their
behavior. Stimuli that come from females, such as sex
pheromones, are far stronger stimuli for them. The
odor of mature females activates males and increases
the demonstration by them of courtship behavior and
sound generation. The visual image of a mature female
has no stimulating effect on the male behavior (Lugli
et al., 2004). The mechanism of sound generation by
gobies, some of which have no swimming bladder, is
unknown (Kasumyan, 2008).
Still another group of vocalizing fish with a drasti
cally pronounced territoriality in the spawning period
are Cichlidae. Inviting sounds, apparently stridulating
ones by their nature and resembling grunts are emitted
by territorial males of Cichlidae. In cichlid Tra
mitichromis intermedius which inhabit the great Afri
can lakes, the vocalization of males takes place in the
968 KASUMYAN
reproduction period and is always observed in connec
tion with the spawning behavior that proceeds simi
larly in many fish of this family: a territorial male
bends its caudal peduncle to the side opposite from a
female, turns its side upon it, quivers with the body,
spreads its unpaired fins, rapidly and interruptedly
flaps with pectoral fins, and slowly moves its caudal fin
during ejaculation of the sperm portion. The duration
of sounds in male T. intermedius is approximately
120–170 ms with approximately 10 pulses in a series
and the dominant frequency of 320–510 Hz. It is
important to emphasize that sounds are heard only
when the male demonstrates precisely such behavior
(in all 1370 recorded cases of sound emission by fish!);
however, it does not always have an acoustical accom
paniment, for instance, if it is produced by nonterrito
rial males (Ripley and Lobel, 2004). This interesting
observation can indicate an intended sound genera
tion in Cichlidae of stridulating sounds generated due
to rubbing of pharyngeal teeth. Observations of terri
torial male Oreochromis mossambicus show that there
is a well pronounced positive relationship between the
frequency of manifestation of reproductive behavior
and sound generation. The presence or absence
nearby of females ready for reproduction does not
affect sound production in these males; they emit
sounds even if a female is absent in the aquarium
(Amorim et al., 2003). As was found in case of species
of the genus Pseudotropheus, cichlid males emit low
and short tonal sounds that resemble moans when
they, on accompanying a female that responded posi
tively to courtships, swim beside it. Moans precede
grunts and a more decisive male behavior. The ampli
tude of moans decreases by the end of this sound,
which indicates that fish are capable of modulating
loudness (Simöes et al., 2008).
Spawning sounds in territorial fish that migrate to
sites of reproduction. Unlike Pomacentridae that
either lead a territorial mode of life or slightly move
within a certain site, some fish form their own spawn
ing sites in biotopes new for them where they get per
forming migrations different in extent. An important
attribute of the activity of territorial males of such fish
can be vocalization, using which they signal that the
site is occupied. The approach to the territory or
entering it by a female ready for spawning or of other
fish drastically increases the emission by the male of
sound signals, as well as causes in it a certain behav
ioral stereotype that depends on a concrete situation.
Among territorial fish that migrate to sites of
spawning, Batrachoididae are most studied. Males of
fish of the genus Opsanus, in spring before the onset of
the spawning period, migrate to the offshore and dis
perse over individual shelters under small fragments of
rocks, stones, and other objects. Males spend several
weeks here—attract females for spawning, guard eggs,
and then early juveniles. Having occupied such a shel
ter, males begin to intensively vocalize, especially with
the onset of evening twilight. Strong typical sounds of
JOURNAL OF ICHTHYOLOGY
males of the genus Opsanus resemble (“buup”); such
sounds are known in English literature as “boatwhis
tle.” The boatwhistle sound is characterized by a high
stereotype and a low level of variability of the main
acoustic characteristics. It is emitted using tympanic
muscles that are well developed in fish. Males of the
genus Opsanus use sounds for attracting females that
ascend the offshore for spawning slightly later than
males. The same sound performs the function of an
agonistic signal using which males show other males
that this territory is already occupied—to males that
have not yet found a free site for spawning or to males
in the neighborhood. It is of interest that the playback
of recordings of such sounds or artificial acoustic imi
tations not only attract females to the sound source,
but also stimulate in males a response vocalization
(Tavolga, 1958a; Gray and Winn, 1961; Winn, 1964,
1972; Fish, 1972). The study of this interesting phe
nomenon, an increase in the response vocalization,
demonstrated that the higher the rhythm of artificial
stimulation of males by boatwhistle sounds, the higher
rhythm of their response vocalization. Of interest is
also the following: the response sounds of males arise
almost always (in 90% of cases) in intervals between
stimulations. The playback of recordings in which
boatwhistle sounds follow each other without an inter
val completely suppresses the acoustical activity in
males (Fish, 1972). Thus, the use of acoustic signals in
fish can be exercised so as to prevent or minimize the
overlapping of sounds of individual fish that vocalize in
common. A similar strategy of acoustic communica
tion is typical also of other vertebrate animals (Zelick
et al., 1999).
The inviting sounds of males of the genus Opsanus
in their structure belong to complex sounds, i.e., to
sounds that consist of a sequence of several simple
sounds. In gulf toadfish O. beta, each boatwhistle
sound begins with one, less frequently, two to three
sounds that resemble grunt and represent short series
of pulses. Grunts have a frequency from 90–110 to
155 Hz and do not belong to tonal sounds, i.e., do not
form harmonics. This component precedes the main
component of a complex sound, a proper boatwhistle
sound that is tonal by nature. Short grunts are consid
ered as a warning signal that will be followed (with an
interval, on average, of approximately 36 ms) by the
main sound component—a boatwhistle that forms
several harmonics. These tonal components that fol
low each other can be, like grunts, several, as in O. beta
or only one, as in another toadfish O. tau. The dura
tion of tonal components that follow each other varies:
usually the first component is considerably longer than
the subsequent. On the whole, tonal components are
characterized by a surprisingly high stability of the
sound frequency that varies within 1 Hz (low modula
tion); in different individuals, the frequency of tonal
components differs more considerably, but, on the
whole, remains in the range of 270 to 290 Hz (Table 1)
(Fine, 1978; Thorson and Fine, 2002a).
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
Table 1. Main acoustic characteristics (M ± m) of sounds emitted by males of oyster toadfish Opsanus tau (Barimo and Fine, 1998)
Sound Sound pressure level, dB
Boatwhistles 126 ± 1.2
Grunts 123 ± 2.3
Note: Sound pressure level was measured at a distance of 1 m from the fish; dB are indicated relative to 1 µPa. M ± m is the average value of
the index and its error.
Grunts can arise not only as signals that precede
the inviting sound of a male, but also in isolation; they
can be generated by males and females. Such isolated
grunts are considered as a second type of sounds from
the repertoire of fish of the genus Opsanus. Isolated
grunts are observed mainly during stress caused, for
instance, by fright. These sounds are also distinguished
by a high stereotype and a low level of variability of the
main acoustic characteristics (Table 1) (Barimo and
Fine, 1998). Isolated grunts can be produced by males
of Opsanus also in response to an increase in the rate of
vocalization of one of the males that competes for a
female and is nearby. In this case, the male as if fixes a
certain acoustic tag or mark to the inviting sound of
the neighbor male, locating it according to the time of
generation within the first tonal component of its
sound. Such behavior was called acoustic tagging and
occurs in almost one third of all sounds recorded at the
spawning grounds in the period of maximum vocaliza
tion of males of Opsanus (evening twilight). Since each
male at some limited site of the spawning ground has
its own individual acoustic specific features, it is
always possible to determine who of them tagged the
sounds of the competitor (Thorson and Fine, 2002b).
Reproduction in another well studied representa
tive of Batrachoididae—plainfin midshipman Porich
thys notatus proceeds in a similar manner. P. notatus is
found in the Pacific Ocean off the coasts of North
America. The ability of these fish to generate sounds is
well known, which was even reflected in its local
names—Californian singing fish, canary fish, and
talkative fish. Mature individuals of P. notatus with the
onset of the reproduction season (the end of spring
and all summer), similar to Opsanus, ascend from the
depth to the littoral where larger males (length of
approximately 15 cm), that are commonly called
males of the first type, dig small shelter nests under
stones. To these nests they attract females (length of
approximately 12 cm) that adhere large eggs (diameter
of approximately 5 mm) to the vault or lateral walls of
the shelter. A female in small portions spawns all eggs
immediately (approximately 200 items), while a male
successively spawns with several females, and the total
number of eggs in one nest can exceed 1000. Smaller
males of P. notatus are present in the littoral during
reproduction. Their length is almost two times smaller
(approximately 9 cm) than in large males, but they
have more developed gonads and a considerably
higher (almost tenfold) gonadosomatic index. Small
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11
969
Basic frequency, Hz Duration, ms
249 ± 5.2 286 ± 15.3
155 ± 5.9 71 ± 2.5
males (males of the second type) have no own nests;
their numbers are small, approximately 10% of all
males per a spawning ground (Brantley and Bass,
1994). These males of P. notatus are sometimes called
petty thieves or sneakers, because they try to penetrate
unnoticed to the nest of a large male when a female
enters it and to participate in spawning. Such behavior
is frequently successful.
The spawning activity of males of P. notatus begins
with the sunset. Males approach the entrance of their
nest and, looking out from it, begin to emit a sound
that resembles monotonous hum (frequency of
approximately 100 Hz) (Fig. 4). A typical specific fea
ture of male hums is their extremely long duration.
Some hums continue without an interval for more
than 10 min, and with small intervals, up to 1 h! The
frequency and amplitude of respiratory movements
with operculi in males at these moments considerably
increase. Using these sounds, males attract females to
the nest, which is well supported by observations of
responses of females to the playback of recordings of
male hums: females rapidly gather near the source of
such sound, turn round it, and bite (Ibara et al., 1983;
McKibben and Bass, 1998). A female that approached
the nest either enters it or it occurs after insistent
nudgings of a male during intervals between hums. As
soon as a female enters the nest or during the first
minute after its coming, a male ceases humming and
blocks the way out of the nest. Pressing a female to the
nest wall, a male performs rhythmic, once per 1–3 s
stereotype blows or slaps with head against the body or
caudal peduncle of a female inducing it for spawning.
Several minutes after, a female assumes a typical pos
ture—it turns abdomen to the wall or vault of the nest
and begins to gradually spawn eggs (Fig. 5). The
spawning process is prolonged and can continue up to
20 h. The female immediately adheres eggs, pressing
them to the substrate; the male every several minutes,
pushing the female to the side, turns up down, and
quivering, emits sperm portion. Having thus emitted
all eggs, the female, on turning abdomen up, freezes
immovably, which is a signal for the male that spawn
ing has ended. The male removes the female from the
nest and remains to guard the spawned eggs. Females
produce no sounds before entering the nest and
throughout spawning.
The spawning that takes place attracts males of the
second type to the nest. They try to penetrate unno
ticed into the nest and, if one of them is successful, it
2009
970
(a)
(b)
500 ms
(c)
Fig. 4. Oscillograms of sounds of plainfin midshipman Porichthys notatus: (a) hum, (b) grunt, and (c) growl. Oscillograms are rep
resented in two time scales (Bass et al., 1999).
either imitates the spawning behavior of a female and,
turning up down, presses itself to the nest walls with its
abdomen, or buries itself into the ground in a difficult
to access corner. When nests of males of the first type
are examined after a female enters them and spawning
begins, these small males are frequently found, in 20–
40% of cases. Males of the second type not only in
behavior, but also in sizes, and body coloration and
shape (increased abdomen) resemble females. Such
mimicry hinders their recognition. However, if a male
of the first type still notices the undesired competitor,
it drives it out. If a male of the second type fails to pen
etrate into the nest or it was driven out, it selects
another tactic: slowly backing its tail forward, it tries to
invisibly approach as much as possible the entrance to
the nest or even penetrate into it partially with a tail,
and then direct to the nest a water flow formed by the
movements of fins, and together with it the sperm that
is periodically ejaculated at this moment. Such behav
KASUMYAN
500 ms
20 ms
20 ms
500 ms
20 ms
ior coincides in time with spawning of eggs by a
4
female. Having noticed a competitor, the male of the
first type immediately attacks the pushy individual. If
it does not occur, the male of the second type remains
near the entrance to the nest throughout the spawning
(hours). At any tactic of participation in spawning,
males of the second type do not court a female and do
not produce inviting sounds, even when a male of the
first type is forcibly driven out of the nest. Although
successful spawning can proceed under such artificial
conditions. Males of the second type are never
engaged in protection of the eggs and the newborn
juveniles. Even if they enter a free nest, they remain
4 Apparently, sex pheromones that get into the water in many fish
together with genital products serve as signals about the begin
ning of spawning that attract males of the second type to the nest
(Kasumyan, 2004). Unfortunately, there are no published data
on sex pheromones in plainfin midshipman.
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH 971

(a) (e)

(b) (f)

(c) (g)

(d) (h)

Fig. 5. Spawning behavior of plainfin midshipman Porichthys notatus: (a) male of the first type in the nest; with the onset of night,
it emits strong inviting dull lowfrequency sounds resembling hums or purrs; (b) a female deposits eggs on the surface of the vault
of the nest, and the male of the first type becomes silent immediately after the female enters the nest; (c) circling and quivering
and the male of the first type inseminates the eggs; (d) a male of the second type that penetrated the nest unnoticed inseminates
the eggs; (e) the male of the second type that stayed before the entrance to the nest directs a water flow into the nest and releases
sperm portions; (f) the male of the first type drives away the male of the second type from the nest; (g) the male of the first type
guards egg batch; with the onset of the next night, it again begins to produce inviting sounds, and the spawning process can be
repeated; (h) the male of the first type widely opens its mouth and emits threatening grunt when another male of the first type
approaches the nest (Brantley and Bass, 1994; Bass, 1996).

there for a short time and prefer to spend most time,
similar to females, burying themselves into the ground.
If males of the first type emit prolonged hums
exceptionally for attracting females to the nest, grunts,
considerably shorter (59 to 200 ms), are produced by
them during agonistic manifestations—when a male
of the second type has penetrated into the nest or if
another male of the first type approaches or enters the
nest, that is usually rather soon driven out by the nest
owner (Fig. 4). Emitting grunts, the male of the first
type demonstrates a threat—a widely opened mouth
directed towards the enemy (Fig. 5) (Brantley and
Bass, 1994; Bass, 1996).

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

972 KASUMYAN

SPAWNING SOUNDS IN FISH THAT
TEMPORARILY PASS TO A TERRITORIAL
MODE OF LIFE IN THE PERIOD OF
REPRODUCTION
Transition to territoriality is also typical of fish that,
beyond the reproduction period, are inhabitants of the
pelagial and open areas of large water bodies, can lead
a typically gregarious mode of life, freely move to large
distances, and have no sites of their own. To these fish
we may relate representatives of Gadidae, for instance,
Atlantic cod Gadus morhua whose males in the
prespawning period and during spawning (February–
March) emit muffled grunts. Females, despite the
presence in them of tympanic muscles, keep silent at
all phases of reproductive behavior; however, they also
can emit sounds sporadically beyond the spawning
season (Engen and Folstad, 1999).
The grunt sound in the cod has a duration of
approximately 200 ms and the basic frequency of
approximately 50 Hz (Brawn, 1961b; Hawkins and
Rasmussen, 1978). Under artificial conditions, to
which adult individuals of the cod easily get accus
tomed and where they can spawn, males with a length
of 50–70 cm emit sounds that humans can here at a
distance of several meters from the basin (Brawn,
1961b). In the daytime, these sounds are heard rarely,
but with the onset of twilight, they are recorded far
more frequently, especially, if spawning takes place in
the basin. Switching of artificial illumination
decreases the frequency of vocalization; after switch
ing off, it increases again. The spawning behavior of
males is initiated by a female ready for spawning of
eggs when it slowly and fearlessly swims to the territory
guarded by a male from other males and immature
females. On noticing a mature female, a male
approaches it with highly raised unpaired fins and
leads it within its territory, swimming aside or around
it by a twisting trajectory, and making numerous
detours and sharp turns. At this time, one can hear
male muffled grunts, to each of which a female
responds immediately by an increase in the rate of
swimming, turns towards the male, and spreads dorsal
fins. For a short time, the male can freeze before the
female, located on its side perpendicular to the direc
tion of its movement (lateral display). The effect of
such demonstrations increases when it is accompanied
by lowering of the first and second dorsal fins and the
first anal fin and then their abrupt spreading. If a
female freezes near the bottom, a male swims under it
and slightly pushes its abdomen by the head, accom

7 6 5

2 4
1

Fig. 6. The spawning behavior of Atlantic cod Gadus morhua: (1) a female enters the male’s territory; (2) the male rapidly
approaches the female with highly spread out unpaired fins and swims in front of it along a complex trajectory (demonstration
behavior); (3) the male leads the female deep into its territory and the female follows the male; (4) a prolonged period during
which the males leads the female upwards, then again descends with it to the bottom, continues demonstration behavior, emits
grunts, and slightly hits the female on the side and on the abdomen; (5) the female following the male, moves upwards and freezes
near water surface, the male presses the female from the top; (6) the male lies above the female, fish slowly move near the water
surface; (7) the male swims up under the female and presses its abdomen to it, spawning. The male’s outline is shaded; a dotted
line designates a boundary separating the male’s territory from the remaining part of the basin where there are several mature
males and females of the cod (according to Brawn, 1961a).

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

 ACOUSTIC SIGNALING IN FISH
Table 2. Main acoustic characteristics of sounds of males of haddock Melanogrammus aeglefinus (Hawkins and Amorim, 2000)
Sound Number of double Duration of the
Sound
duration, s pulses in a sound double pulse, ms
Short slow 0.8 3.8 25.5
Short rapid 1.3 12.6 25.2
Long slow 3.1 14.5 26.3
Long rapid 9.0 58.5 24.9
Humming 8.3 – 24.3
panying pushes with a loud grunt. In response to such
actions, the female accompanied by the male performs
an upward migration to the water surface where
spawning soon takes place. At the moment of synchro
nous spawning of genital products, the male is under
the female, turning back down and pressing itself to
the female abdomen (Fig. 6). At the terminal phases of
the spawning behavior when fish ascend to the water
surface, sounds are not generated (Brawn, 1961b).
The number of successful spawnings in male Atlantic
cod closely correlates with the sizes (weight) of tym
panic muscles and is not related to their body length,
fatness, or fin sizes (Rowe and Hutchings, 2008). It
was noted that sound emission by male cod ceases the
spawning behavior of another male directed at it. If a
territorial male erroneously exhibits a courtship
behavior with respect to an immature female or a
female with spawned eggs, it is interrupted immedi
ately after the beginning of emission of sounds by the
male that cause, in a female, a rapid departure
(Brawn, 1961b). At the spawning grounds of the
Atlantic cod (the Lofoten Islands), during spawning,
the sounds of many fish fuse in a single rumble that is
well heard using a hydrophone; beyond the spawning
season, no sounds are heard at sites of the cod aggre
gation (Nordeide and Kjellsby, 1999). The acoustical
repertoire of the cod used by it in nature, can, as is
assumed, not be limited to only one grunt sound, but
be more diverse (Midling et al., 2002; Finstad and
Nordeide, 2004).
Acoustic signaling during spawning is typical not
only of G. morhua, but also of other representatives of
this family—walleye pollack Theragra chalcogramma
and lythe Pollachius pollachius (Hawkins and Rasmus
sen, 1978). However, the most complex acoustic sig
naling among studied Gadidae is apparently in had
dock Melanogrammus aeglefinus. The repertoire of
male haddocks includes five different sounds that sub
stantially differ in the number of double pulses in the
sound, frequency of sequence of double pulses, and
sound duration. The duration of each double pulse
and the interval between pulses, as well as the values of
the peak (dominant) frequency of these sounds differ
weakly (Table 2). Humans perceive these sounds as
knocks that, in the haddock, depending on the situa
tion, change from relatively short and slow knocks to
rapid and prolonged. The sound in which knocks fol
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
973
Interval between Interval between Dominant
double pulses, ms pulses, ms frequency, Hz
397 13.5 253.5
105.5 12.6 203.7
217.7 13.6 220.6
87.7 12.0 197.2
30.3 11.1 184.7
low with a very high frequency (each 30 ms) resemble
humming. The spawning behavior of haddock in some
elements resembles cod behavior; however, the acous
tic accompaniment of this behavior differs substan
tially more strongly. Haddock males ready for repro
duction when kept under artificial conditions periodi
cally descend to the basin bottom and begin to swim
along circular or Sshaped trajectories with a small
radius. At this moment, they can change pigmenta
tion—at the lateral surface two additional pigmental
spots can appear, usually behind the usual one typical
for this species (Fig. 7). Such swimming is interpreted
5
as the manifestation by a male of a territorial behavior
and is called solitary display. Solitary display is accom
panied by emission of sounds—prolonged rapid and
slow series of knocks that, as is assumed, serve as a sig
nal of male preparedness for spawning, according to
which females select a male at the spawning ground.
The existence of nonrandom, selective choice of sex
ual partners in Gadidae is supported by genetic studies
(Hutchings et al., 1999).
If a haddock female is absent nearby, the male can
return to more or less quiet swimming in the water col
umn and slower swimming over the bottom, touching
it with rostrum and ends of pectoral fins (a tripod pos
ture). If a female responds to the male’s invitation and
approaches it, the male moves to it and, following it at
a small distance (approximately one half of body
length), performs several so called lateral demonstra
tions with highly raised unpaired fins, accompanying
demonstrations by emission of almost the whole set of
sounds. If the female does not go away and continues
to stay with the male, this initiates in it the subsequent
development of courtship behavior: the male stands
perpendicular in the way of the female and begins
flicking fins. At this time, additional pigmental spots,
the same as in solitary display can appear on the male’s
body. The frequency of knocks in sounds emitted by
the male at this time increases all the more and can
5 In haddock males, however, no behavior directly associated with
the protection of the territory from other fish was found (Hawk
ins and Amorim, 2000; Bremner et al., 2002). This can be sup
ported also by results of acoustic surveys at the spawning
grounds of haddock, according to which, during the light hours
of the day, these fish form aggregations that stay above the bot
tom. With the onset of night, fish descend to the bottom, and
aggregations break down (Boudreau, 1992).
974 KASUMYAN
(a)
(c)
Fig. 7. Elements of spawning behavior of haddock Melanogrammus aeglefinus: (a) solitary display, (b) sharp openings and lower
ings of unpaired fins by a male that stood perpendicular in the way of a female (flicking), (c) lateral display, and (d) mating
embrace. The male’s outline is shaded (Hawkins and Amorim, 2000).
reach maximum level. Then the male again follows the
female, being near it, pushing it by the rostrum, and
whirling around it. As a result of such actions the male
and female, having ascended upwards, position hori
zontally and closely press to each other by abdomens
with entangled ventral fins. This posture was named
mating embrace (Fig. 7). At precisely this moment,
spawning occurs—simultaneous spawning of eggs and
sperm. After sperm release, sound emission ceases
immediately. Thus, as the spawning behavior devel
ops, the male emits sounds more frequently, and max
imum of sound generation is reached towards the
moment of liberation of genital products. Sounds with
maximum frequency of knocks in haddock has also
maximum average duration, up to 10 min (!) (Hawkins
et al., 1967; Hawkins and Amorim, 2000). Haddock
males generate sounds in the daytime and at night, but
only in the case if a mature female is present together
with them in the basin. When males are kept in isola
tion, they do not generate sounds, which may indicate
the absence in them of competition for the territory. At
the same time, when still another male is placed to the
spawning pair, sound generation increases (sound
duration increases by 2–4 times), which does not
allow to exclude the presence of competition between
haddock males for a female (Bremner et al., 2002).
Apparently, in haddock, as in the closely related
Atlantic cod, the leading role of the dominant male in
the struggle for a female is pronounced more strongly
in fish groups large in numbers (Hutchings et al.,
1999), while, in small groups, several competing males
can simultaneously participate in spawning (Rakitin et al.,
2001). It is necessary to stress that in all these studies,
observations of reproduction were made in captivity
JOURNAL OF ICHTHYOLOGY
(b)
(d)
when area deficiency and a prolonged joint keeping of
experimental fish could distort their behavior. In gen
eral, the role of acoustic signaling in the spawning
behavior of haddock and other representatives of
Gadidae stresses the fact that the reproduction of
many of these fish takes place in winter time at night at
a relatively large depth (more than 100 m) at northern
latitudes, i.e., under conditions where possibilities for
visual reception are limited. The sizes of tympanic
muscles in these fish towards the reproduction season
increase by more than twofold (Templeman and Hod
der, 1958).
Most Cyprinidae belong to fish that, outside the
reproduction season, lead a migratory mode of life.
Many of them do not exhibit a territorial behavior in
the reproduction period either. However, there are
Cyprinidae whose males at this time pass to a typically
territorial behavior, for instance, North American
Cyprinella galctura, Codoma ornate, and Pimephales
notatus. Males of precisely such Cyprinidae emit
sounds in the spawning period (C. Johnston and
D. Johnston, 2000b); Johnston and Vives, 2003; Phil
lips and Johnston, 2008a). In the aquarium, male
C. ornate emit sounds that resemble bursts. The males
emit them during courtship when they try by their
swimming before the entrance to the shelter crevice to
attract a female to it. The same sounds are audible dur
ing spawning. The mechanism of generation of such
sounds is unknown. Females produce no sounds
(Johnston and Vives, 2003).
The territorial males of North American fish that
belong to the family Percidae—Etheostoma nigripinne
and E. crossopterum emit sounds that resemble
knocks, purrs, and drums. These sounds arise only in
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH 975

Table 3. Acoustic parameters of sounds emitted by territorial males of Etheostoma nigripinne and E. crossopterum at aggressive
contacts, during courting a female, and spawning (C. Johnston and D. Johnston, 2000a)
Sound parameters Parameters of sound pulses
Sound type
and behavioral form dominant pulse
occurrence, % duration, ms number duration, ms
frequency, Hz frequency, s
E. nigrippine
Drumming:
courtship 77 129 ± 35 740 ± 420 – – –
aggression 87 146 ± 28 580 ± 260 – – –
total 83 139 ± 32 640 ± 340 – – –
Knocks, total 10 104 ± 32 380 ± 310 1.9 ± 1.3 5.6 ± 1.0 230 ± 100
Purring, total 7 89 ± 62 350 ± 220 6.4 ± 3.1 19.1 ± 5.1 60 ± 20
E. crossopterum
Drumming:
courtship 72 77 ± 9 960 ± 310 – – –
aggression 83 90 ± 9 600 ± 310 – – –
spawning 74 93 ± 16 740 ± 340 – – –
total 78 89 ± 13 730 ± 330 – – –
Knocks:
courtship 28 100 ± 20 600 ± 510 – – –
aggression 17 95 ± 20 460 ± 160 – – –
spawning 26 99 ± 15 570 ± 400 – – –
total 22 98 ± 18 530 ± 350 1.9 ± 0.9 4.4 ± 1.8 270 ± 110
Hybrid of E. nigrippine and E. crossopterum
Drumming, total 92 102 ± 19 690 ± 470 – – –
Knocks, total 8 105 ± 22 480 ± 250 1.3 ± 0.5 2.3 ± 0.9 390 ± 100

connection with reproduction and are audible during
aggressive encounters of males with competitors, dur
ing attraction of a female to the nest, and during
spawning. Drumming sounds are most common
(Table 3). Sounds arise irrespective of the fact whether
fish are in the nest or outside it. During spawning,
sounds arise immediately before spawning of eggs by a
female or at the moment of spawning. Males are silent
in intervals between fights and in the absence of a
female nearby that stimulates courtship behavior.
Sound generation by females was not established. As
in the case of C. ornate, uniform sounds in Etheostoma
during manifestation of different forms of behavior
differ in frequency and duration, which indicates the
presence in fish of a capability to modulate acoustic
parameters of the sound depending on the concrete
context of behavior (Table 3) (C. Johnston and
D. Johnston, 2000a). This specific feature seems to us
extremely important for acoustic communication and
exchange by acoustic signals that have precise address
and situation destination.
Spawning sounds in nonterritorial resident fish.
Sounds related to the spawning season are generated
not only by territorial fish or fish that temporarily pass
to territoriality for this period, but also by fish that do
not stay only in certain sites even if their movements
are not so considerable. Among such fish is cuskeel
Ophidion marginatum—a small marine fish that
inhabits waters off the coasts and spends the light
hours of the day burrowing itself into the ground.
Acoustic communication in the cuskeel is rather
peculiar. Males begin to emit sounds (series of 1–
27 sound pulses with a frequency of 500 to 1800 Hz)
even when they are in the ground, before the onset of
twilight. When a cuskeel leaves the ground, vocaliza
tion increases and rapidly reaches maximum. Females
in response to male sounds also begin to quit the
ground and swim more actively, and, moving by cir
cles, try to determine the sound source. The period
during which males emit sounds is relatively short; it
begins approximately 40 min before spawning,
includes the moment of spawning genital products,
and terminates 15–20 min after it. In males, sound
generation is accompanied by head quivering and, in
females, by vibration of pectoral fins (Mann et al.,
1997; Rountree and BowersAltman, 2002). Record
ing sounds, it is possible to find habitats of these little
noticeable fish, perform monitoring of the state of

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

976 KASUMYAN

Amplitude, mV
+ (a) Pollimyrus isidori
0

Frequency, Hz 1

1 3 5
Amplitude, mV

(b) Pollimyrus adspersus

+

0
_

2
Frequency, Hz

0 1 3 5 7 9 11
Time, s

Fig. 8. Oscillogram (above) and sonogram (below) of complex sounds emitted in the spawning period for attracting females by
males of (a) Pollimyrus isidori and (b) P. adspersus (according to Crawford and Huang, 1999; Lamml and Kramer, 2005).

their populations, and elaborate measures for the pro
tection and recovery of their stock (Rountree et al.,
2006).
Another example of fish that, similar to the cusk
eel, use acoustic signaling under conditions when pos
sibilities of visual reception are limited can be weakly
electric African fish Mormyridae. These fish possess
socalled auditory or tympanic vesicle that is closely
adjoined to the saccular sac and belong to a group of
auditory specialists (Kasumyan, 2005). Mormyridae,
in particular, fish of the genus Pollimyrus (P. marianne,
P. adspersus, and P. isidori) spawn in the dark hours of
the day; their reproduction season is in the season of
rains when water turbidity becomes high. This limits
the function not only of vision, but of other systems
also. For spawning, male Pollimyrus construct nests of
plant material, usually near the bottom in shelters.
With the onset of the reproduction season, the acous
tic activity of male Pollimyrus directed at attracting
females to the nest successively increases and reaches
maximum during the spawning night, and then, dur
ing protection of the batch and hatching of larvae,
decreases and ceases after juveniles leave the nest and
begin to swim and feed independently. During a sea
son, several successive spawning cycles pass in
Polimytrus; therefore, males after some time begin to
vocalize again. The sounds of males of Pollimytrus
belong to a category of complex sounds, they consist of
several simple sounds that follow in different order in
different species and have different acoustic character
istics (Fig. 8) (Table 4). In the absence in close vicinity
of a female or other fish, males of P. isidori emit moans
sporadically. When a female approaches the nest, the
male responds to its electric discharges by prolonged
moans and grunts overlapping them (Crawford et al.,
1997a, 1997b; Lamml and Kramer, 2005). In the

Table 4. Some acoustic characteristics of simple sounds of the moan and grunt types in males of the genus Pollimyrus (according
to Crawford et al., 1997)
Moan Grunt
Species peak fre peak fre frequency of pulse
duration, ms duration, ms
quency, Hz quency, Hz sequence, Hz
P. marianne 1897 175 561 1076 34 Lamml and Kramer, 2005
P. adspersus 812 240 229 – 56 Crawford et al., 1997a
P. isidori 121 332 268 – 44 ″

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

 ACOUSTIC SIGNALING IN FISH
experiment, in order to cause in a male inviting
sounds, it is sufficient, imitating a female presence, to
reproduce its electric signals. Such stimulation not
only leads to a response vocalization, but is also
accompanied by typical behavior (Crawford, 1991).
Beyond the reproduction season, when other fish
approach, males emit moans and, rarely, grunts that
differ in acoustic characteristics from sounds gener
ated by them in the spawning period during courtship
of a female (Lamml and Kramer, 2005).
Stridulation clicks are emitted by lined seahorses
Hippocampus at courtship display and during copula
tion; basic frequency of these sounds embraces a range
of 400–800 Hz (Fish and Mowbray, 1970).
Spawning sounds in nonterritorial migratory fish.
Sciaenidae belong to the most known vocalizing fish
that do not exhibit territoriality and retain a migratory
mode of life throughout ontogenesis. Their acoustic
activity is also related to the reproduction period. For
instance, gray weakfish Cynoscion regalis at this time
(May–July) forms dense spawning aggregations off
the coasts of the Atlantic coasts of North America. At
the same time precisely in the offshore rather than in
the open sea, drumming sounds emitted by males of
these fish are registered. Maximum sounding occurs at
the peak of the spawning when the proportion of indi
viduals with ripe genital products is highest in catches.
The diurnal cyclicity of acoustic activity and spawning
also coincide. Beyond the spawning season, males of
the gray whitefish do not generate drumming sounds
(Connaughton and Taylor, 1995).
With the onset of the spawning season, the behavior
of males of Sciaenidae changes; however, no transition
to actual territoriality and selection and protection of
individual territories occurs. Audio and video observa
tions in basins show that males of gray whitefish ready
for spawning with the onset of evening twilight when
spawning takes place stay immovably above the bottom
and, almost not stopping, emit drumming sounds. Any
competitive relations between males are absent. As
soon as a female appears nearby, the male becomes
silent, swims to it, nudges, and follows it up to the sur
face where paired spawning that lasts only for several
seconds occurs. During spawning of genital products,
fish do not emit sounds. After spawning, the male
again descends to the bottom at an accidentally
selected place, and a new cycle begins. The total time
of vocalization and spawning varies from 2 to 3 h
(Connaughton and Taylor, 1996). In a natural envi
ronment, closely spaced males of gray whitefish emit
sounds apparently alternately (Connaughton and Tay
lor, 1995). Males of other species of Sciaenidae (Sci
aenops ocellatus, Argytosomus regius, and Micropogo
nias undulatus) behave similarly (Guest and Lasswell,
1978; Connaughton and Taylor, 1995; Lagardère and
Mariani, 2006). Males of Sciaenidae emit sounds, as is
assumed, to form spawning aggregations and attract
females. Since the acoustic specific features of sounds
depend on the body size of the vocalizing male, it is
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
977
quite probable that a female selects males according to
their sounds and prefers males that produce sounds
higher in amplitude and lower in frequency (Con
naughton et al., 1997, 2000). Sounds can help other
fish also to form spawning aggregations (Templeman
and Hodder, 1958; Connaughton et al., 2002a).
The spawning sounds of Sciaenidae are produced
using tympanic muscles and embrace a frequency
interval of 100 to 1000 Hz with maximum amplitude in
the range of 250–600 Hz. Harmonics in them, oppo
site to drumming sounds of many other fish, are absent
(Ramcharitar et al., 2006). Sounds in Sciaenidae are
rather prolonged—in gray weakfish their duration
reaches 500 ms (Connaughton et al., 2002b). In
A. regius, spawning grunt sounds are still more pro
longed—from 0.6 to 2.5 s; they represent long series of
30–110 pulses, their frequency range is 340–445 Hz.
Males of A. regius emit such sounds, on average, 12–
13 times per minute; their peculiar singing stops
immediately after a short grunt with a duration of less
than 100 ms that is recorded at a female approach. It is
unclear who emits this short acoustic signal, a male or
a female. It is assumed that it may be produced by a
male when it rushes to a female that approached it or
a female signaling in this way that it is ready for spawn
ing and inviting the male (Lagaedère and Mariani,
2006).
The territorial behavior not only in connection
with reproduction, but also in other periods of life is
also not exhibited by vocalizing fish such as peppered
corydoras Corydoras paleatus. Several males of C. pale
atus can simultaneously participate in the courtship of
a female; antagonistic or obviously aggressive manifes
tations between males are lacking. The courtship
behavior of males manifests itself in following a
mature female and in periodic emission by them of
stridulation sounds. Courtship terminates by fixation
by one of the males of a female in so called Tposi
tion—for this, it presses the barbels of the female by its
pectoral fin and holds it in such position for several
seconds (13 ± 0.3 s), during which spawning of genital
products takes place (Fig. 9). In C. paleatus, the
moment of emission of stridulation sounds is clearly
identified according to rapid movements in succession
by right and left fins. Each movement of the fin for
ward (abduction) leads to the generation of one simple
sound; simple sounds that follow each other form a
series. On average, the duration of one simple sound in
a series is approximately 17 ms, the interval between
sounds is 33.5 s, the number of sounds in a series is
approximately 30, and the duration of the whole series
is approximately 1.25 s (Fig. 10). Females do not pro
duce sounds during courtship behavior and spawning
(Pruzsinszky and Ladich, 1998).
Among fish that do not exhibit obvious territorial
ity, there are also some fish of coral reefs that spawn
eggs not on the substrate, but disperse them in the
water column. Their spawning behavior can be also
accompanied by emission of sounds that regulate
978 KASUMYAN

behavior and synchronize spawning. This signaling is

(a)
(b)
Fig. 9. Successive phases of spawning behavior in Corydo
ras paleatus: (a) two males ( ) pursue a female larger in its
sizes ( ), a male staying above a female vocalizes; (b) a
male keeps a female having pressed its maxillary barbels by
its pectoral fin, the spawned portion of eggs is in the folded
down female fins (Pruzcinszky and Ladich, 1998).
complex and interesting in synchronous hermaphro
dyte Hypoplectrus unicolor (Serranidae) that belongs to
monogamous fish: individuals that form a pair, succes
sively with a small interval, participate in spawning
acting as a female when spawning a portion of eggs, or
as a male when inseminating the spawned eggs.
Sounds are generated by both fish, i.e., a “male” and a
“female,” but they emit sounds of different type and at
different moments of spawning. A fish that acts as a
male generates a sound with a frequency of approxi
mately 500 Hz and duration of 0.2–1.5 s at the termi
nal phase of courtship behavior several seconds before
own spawning—at the moment when the “male”
closely twines itself round the partner that performs
the role of a female in this cycle. At the moment of
proper spawning, i.e., at the liberation of eggs, the
sound is emitted by a “female” quivering by its pecto
ral fins. Fish, at this time, are directed to opposite
sides, which, as is assumed, decreases the probability
of seizing of them by predators, in which in the
evening hours when spawning occurs, maximum feed
ing activity is observed. The sound of a “female” lasts
approximately 1.5 s and has a peculiar structure. The
first part of the sound is short, it lasts approximately
0.15 s. During this time, the sound frequency
decreases from 600 to 200 Hz, and then after a small
interval, a substantially prolonged and wide in frequency
second part of the sound follows (350–1650 Hz). The
first part of the sound is considered as a signal sent by
a “female” to a “male” of the beginning of spawning
eggs and intended for synchronization of spawning.
The second part of the sound, apparently, has no signal

(a)
Frequency, kHz

50 100 150

(b)
Amplitude

50 100 150
Time, ms
Fig. 10. (a) Sonogram and (b) oscillogram of sounds emitted by males of Corydoras paleatus during courtship of the female
(Pruzsinszky and Ladich, 1998).

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

 ACOUSTIC SIGNALING IN FISH
Table 5. Sounds of pallid sturgeon Scaphirhynchus albus and shovelnose sturgeon S. platorynchus emitted in the reproduction
period (average values) (according to Johnston and Phillips, 2003)
Pallid sturgeon
Sound proportion
dominant fre duration, number
from all
quency, kHz ms of harmonics
sounds, %
Squeak 0.92 211.1 3.2 51
Chirp 2.0 71.2 2.0 17
Knock 0.16 196.6 none 24.5
Moan 0.37 210.8 none 7.5
function and arises in connection with the locomotor
activity of the female during spawning—with flicker
ing flaps of pectoral fins and frequent contractions of
abdominal musculature. Immediately after spawning
of genital products, fish abruptly move to opposite
sides and move downwards to the reef. Such spawning
cycles can repeat multifold with a periodicity of several
minutes (Lobel, 1992).
Spawning in another nonterritorial fish of coral
reefs—gregarious parrot fish Scarus iserti (Scaridae)—is
group, and up to several tens of individuals can partici
pate in it simultaneously. Directly before spawning, fish,
having assembled in a dense group, almost simulta
neously make a rapid dart several meters upwards and, on
reaching the upper point of the dart, spawn genital prod
ucts and then instantaneously return back. The frame
analysis of spawning recordings shows that a dart is usu
ally performed by these small fish (maximum body length
of 30–35 cm) with a rate of approximately 12 m/s! The
route upwards to the spawning point occupies 200 to
400 ms; the same time is required by fish also for return
downwards to the reef; the whole cycle takes approxi
mately 1 s (Colin, 1978). The route of fish upwards and
downwards is accompanied by a broadband sound (350–
1650 Hz), that has apparently a hydrodynamic nature
(Lobel, 1992). The signal function of this sound seems
questionable. It is also unclear how such high coordina
tion of rapidly occurring spawning behavior in S. iserti is
reached.
Spawning sounds in nonterritorial migratory fish.
Nonterritorial fish that perform extended spawning
migrations include Acipenseridae that are representa
tives of Chondrostei—an ancient group of Osteich
thyes. These fish begin to emit sounds before the start
of spawning when they, having overcome considerable
distances during their spawning migration, aggregate
at the spawning grounds. In the remaining time, Aci
penseridae emit no sounds. In pallid sturgeon Scaphi
rhynchus albus and shovelnose sturgeon S. platoryn
chus, sounds in the spawning period are emitted not
only by mature males, but also by females. The ampli
tude of these sounds is sufficient to be audible in air
above basins with fish. It is of interest that sounds in
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
979
Shovelnose sturgeon
proportion
dominant fre duration, number
from all
quency, kHz ms of harmonics
sounds, %
1.3 112.3 3.9 54
2.1 57.6 2.3 37
0.09 230.9 none 8
0.26 100.0 none 1
these, as is considered, asocial fish arise in the case if
several experimental fish are placed simultaneously in
the basin for observations. Sounds in solitary fish are
recorded extremely rarely. A total of four basic types of
sounds that are equally typical of individuals of both
sexes were distinguished. In more than a half of cases,
a squeak sound occurs; in two species of Scarphirhyn
chus, this sound differs in the dominant frequency,
duration, and the number of harmonics (Table 5). It is
suggested that squeak and another highfrequency
sound, chirp, can be used by fish at short distances
when selecting a sexual partner or for individual
recognizing individuals at the spawning grounds.
Lowfrequency sounds like knock or moan that are
better distributed in water can be used for distant
communication, for instance, for attracting mature
individuals of own species to the spawning sites.
The mode of sound generation by sturgeons
remains unknown. The presence of harmonics in
the squeak sound can indicate the participation of
the tympanic mechanism in its generation
(Johnston and Phillips, 2003), although, there is no
evidence on the presence of tympanic muscles in
Acipenseridae.
Sounds are emitted during spawning by still
another North American sturgeon Acipenser fulve
scens, whose spawning behavior in nature has been
comprehensively described. Spawning of this fish
takes place in the offshore of small rapid rivers. At the
moment of spawning, one of the males (there may be
several) stays slightly in front of a female so that its
caudal fin touched the abdomen of the female from
below or was very near it. By rapid flaps of the caudal
fin (4–5 times per second), the male stimulates the
female for spawning eggs. In time with tail knocks,
typical muffled sounds that resemble distant thun
der growls or flapping of big birds, such as geese or
partridge, are audible above water. By sounding,
these sounds resemble “wumps.” A human that
stands on the shore near spawning fish, together
with sounds, distinctly feels vibration passing
through the ground. Spawning sounds immediately
attract other males that are downstream that rapidly
swim to the spawning site from a distance of 3–
980
6
5 m. The same sounds are emitted by males when
they stay separately from spawning fish, at some dis
tance from them, and as if imitate spawning by typical
movements of caudal fin and release of a portion of
sperm (Bruch and Binkowski, 2002). The acoustic
characteristics of males of A. fulvescens remain
unstudied.
It is reported in literature that mature individuals
also of other Acipenseridae—A. gueldenstaedtii,
A. sturio, Huso huso, and several other are capable of
emitting sounds (Protasov and Romanenko, 1962;
Kirschbaum et al., 2001; Tolstoganova, 2001). It is also
reported that they generate sounds of the “whistle”
type, whose frequency, according to available data, is
extremely high, up to 18–20 kHz (Kirschbaum et al.,
2001; Tolstoganova, 2001), which is considerably
higher than in sounds of almost all other studied fish.
Maximum generation of “whistles” in Acipenseridae
remains unclear.
Thus, vocalization attributed to the reproduction
period is typical of fish different in systematics, mode
of life, and behavior. Among fish that generate spawn
ing sounds, most number of species belongs to either
actually territorial fish or to fish that exhibit territori
ality only in the reproduction period. The number of
nonterritorial fish that emit sounds in relation to
spawning is small. A close correlation between territo
riality and a capability to produce spawning sounds
undoubtedly stresses the importance of acoustic sig
naling for preserving by fish of their own sites, refuges
or shelters, and here located nests and substrate sites
prepared for spawning eggs. Distant signaling using
sounds enables territorial fish that permanently stay at
their own sites and are engaged in standing up for their
rights for them not only to inform competitor conspe
cifics about their presence and occupation of the terri
tory, but also to report individuals of the opposite sex
that they are ready for reproduction. Only in presence
of an efficient distant signaling, territorial fish can be
successful in reproduction and transfer of their own
genetic material to the subsequent generation.
Spawning sounds are typical in most cases only of
males. In most species, females in the reproduction
period, as in the remaining seasons of the year, keep
silent. There is a small number of exceptions to this
rule, for instance, Neogobius melanostomus, in which a
female responds by weak sounds to male courtship or
a synchronous hermaphrodyte Hypoplectrus unicolor,
in which acoustic signals are produced by both nuptial
partners—one that acts as a male, and another that
acts as a female (Protasov et al., 1965; Lobel, 1992).
The inviting sounds or sounds emitted by males during
courtship usually rarely cause in females strong or spe
cific behavioral responses. If acoustic signals are pre
6 One
cannot exclude the fact that the attraction of males to the
spawning site is stimulated by sex pheromones released by
females into water together with ovarian liquid and eggs, rather
than by the sounds of males Kasumyan, 1993)
KASUMYAN
sented in isolation, in the male absence, in most spe
cies, females turn out completely indifferent to such
sounds, as, for instance, in bicolor damselfish (Myr
berg, 1980). One of few exceptions is Bathygobius
soporator, for whose females only sound stimulation is
sufficient to cause in them responses exhibited during
male courtship (Tavolga, 1956).
Male sounds are intended mainly for attracting
females and for their stimulation for spawning during
courtship. Directly before spawning or at the moment
of spawning genital products when synchronization of
actions of partners in spawning is required, sound gen
eration was revealed only in a relatively small number
of species, for instance, in cuskeel O. marginatum,
H. unicolor, and some other fish (Lobel, 1992; Lobel
and Mann, 1995; Lugli et al., 1995; Mann et al., 1997;
Hawkins and Amorim, 2000). In haddock, during
reproductive behavior, a successive increase of sound
generation with maximum at the spawning point
occurs (Hawkins and Amorim, 2000), which indicates
a special importance of sounds in the behavior of fish
of this species. It is important to note that it is not a
rule common for all closely related species, since in
Atlantic cod, the dynamics of sound generation differs
from that in haddock (Brawn, 1961b; Hawkins and
Amorim, 2000). In Acipenseridae that have a poorly
developed visual reception, sound generation is
observed apparently only at the moment of spawning
or reaches by this time a noticeable level (Bruch and
Binkowski, 2002). In fish, in which no sound genera
tion occurs directly before spawning or at the moment
of spawning genital products, synchronization of
actions of nuptial partners is reached, apparently, at
the expense of signals of another nature—visual, tac
tile, or perceived by the sensory organs of lateral line or
by the electroreceptor organs (Moller, 1995;
Kasumyan, 2003, 2004).
Complex forms of behavior, such as reproductive
one, cannot be based on information coming via only
one sensory canal. Signals regulating complex forms of
behavior have a different nature, and their reception is
related to the functioning of different sense organs.
The role and importance of individual sensory systems
in the regulation of reproduction differs in different
fish and depends on specific features of their mode of
life and behavior. The regulating role of sensory sys
tems depends also on a particular phase of the repro
ductive behavior and is determined by their range. For
instance, spawning sounds in many cases exercise dis
tant signaling, while at short distances, the dominant
importance in the regulation of fish behavior can pass
to signals perceived, for instance, by vision and/or lat
eral line (lateral demonstrations, swimming of the
male around a female along a complex twisting trajec
tory, folding and unfolding of fins). In the males of
Atlantic cod, in which the use of such signals is clearly
pronounced, a positive correlation between the sizes of
unpaired fins and the size of spermatocrite is observed
(Brawn, 1961b; Engen and Folstad, 1999).
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
Amplitude
1000 200
Fig. 11. Oscillograms of sounds emitted by males of Hawaiian dascyluus Dascyllus albisella at display of aggressive and reproduc
tive behavior: (a) signal jumps, (b) cleaning of the nest substrate, (c) at entering of a female of the territory, (d) during spawning,
(e) during display of aggression with respect to fish of other species and emitting pops, and (f) at aggression with respect to indi
viduals of the own species and producing chirps (Mann and Lobel, 1998).
Territorial Behavior
Territorial behavior regulates spatial relations
between animals, their distribution over the territory.
This form of behavior is usually accompanied by the
choice or occupation by animals of their own sites and
their protection from competitors. In most cases, such
activity is accompanied by the demonstration or emis
sion by the host of the site of different warning signals
informing that the territory is occupied (agonistic sig
nals) or by direct conflicts between the host and the
pretender to the site (aggression). Agonistic and
aggressive manifestations serve as typical features of
behavior of territorial animals. In many fish, territori
ality and, correspondingly, agonistic and aggressive
behavior are drastically aggravated in the reproductive
period. The capability to form own sites and defend
them from competitors enables such fish not only to
survive, but also to be successful in reproduction. In
connection with this, in this section of the paper, the
role of sounds in the territorial behavior of fish is con
sidered mainly with reference to fish in the period of
their reproduction.
The role of sounds in the territorial behavior of fish
in the period of reproduction. In territorial fish living in
colonies in the tropics and where the spawning season
embraces most or greater part of the year, interactions
between individuals represent a constant change of
behavioral types, when agonistic or aggressive mani
festations are rapidly replaced by the demonstration of
courtship behavior, and on the reverse. Such fish that
exhibit a complex territorial and spawning behavior
and use acoustic signaling include Pomacentridae
(Myrberg, 1972; Kenyon, 1994). Observations and
experiments performed in colonies of bicolor damself
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11
981
(a)
(b)
(c)
(d)
(e)
(f)
300 400 500 600 700
Time, ms
ish show the importance of acoustic signaling in the
territorial behavior of these small coral fish. It turned
out that if the host of the territory is removed, it will be
occupied by neighbors upon several minutes. How
ever, if over the unprotected territory, sounds of its
former host are reproduced, in this case the penetra
tion of other males occurs considerably later than in
the absence of sounds. According to laboratory exper
iments, the territory devoid of the host is much more
rapidly occupied if sounds of other males of the colony
rather than of its former host are transmitted, which
indicates an individual acoustic signature in fish and
their capability to remember such specific features of
acoustic signals. The most difficult thing for intruding
neighbors during penetration to an alien territory is to
make a decision to cross the boundary: on passing this
boundary, the new male spends nearly the same time
to reach the shelter of the former male both at sound
translation and without it. The host of the site returned
to the former site completely restores its rights during
2 min. If the host is left at its site in a glass vessel that
prevents sound distribution, the occupation of the ter
ritory by aliens occurs rarely. Thus, the visual presence
of the host is much more important than an acoustic
one. However, a prolonged maintenance of the own
site is impossible without simultaneous visual and
acoustic signaling (Myrberg and Riggio, 1985; Myr
berg, 1997). Still another evidence of the importance
of sounds in competition of fish for the territory are
experiments performed on Botia horae (Cobitidae).
Botias artificially devoid of the ability to produce
sounds cannot protect their shelter from the interven
tion of other fish, despite the manifestation of agonis
tic behavior, while intact or fallaciously operated fish
easily draw out the invader (Valinski and Rigley, 1981).
2009
982
Amplitude
20
Fig. 12. Oscillogram of double pulses in sounds of males of damselfish Abudefduf luridus (Santiago and Castro, 1997).
In Pomacentrid fish Hawaiian dascyllus Dascyllus
albisella, sounds are emitted by males and females. If
females in Hawaiian dascyllus perform it only at man
ifestation of aggression (pursuit of immature individu
als), males vocalize in more diverse situations—at
manifestation of aggression, at cleaning substrate for
spawning, at attracting and courting a female, and
during spawning. In general, the repertoire of Hawai
ian dascyllus is extremely wide for fish, it includes up
to six sounds differing in the number of pulses, their
duration, and amplitude (Fig. 11) (Mann and Lobel,
1998). The sounds of aggression in the males of
Hawaiian dascyllus are of two types—short sounds
consisting of one to two pulses and resembling an
abrupt crack, pops, and more prolonged chirps con
sisting on average of five to six pulses. Males emit
abrupt crack and pops more frequently when fish of
other species (Cheilinus unifasciatus, Epibulus insidia
tor, Chaetodon lunulatus, Forcipiger flavissimus, Ostra
cion meleagris, Ctenochaetus atrigosus) penetrate to
their territory; many of them can represent a direct
danger or for proper males or for the batch of eggs
guarded by them. It is of interest that the same sounds
are emitted by males at the approach of a scuba diver
observing fish. More prolonged chirps sounds are usu
ally heard when a male of the same species—a direct
competitor for the territory appears nearby (Mann and
Lobel, 1998). It should be stressed that a successful
protection by a male of its territory is reached not so
much owing to the generation of warning sounds as
due to visual signaling. Specific elements of behavior
of males of Pomacentridae such as signal jumps and
dips serve, as is assumed, as elements not only of
reproductive, but of agonistic behavior also since they
are observed when males try to attract a female that
appeared or when females are out of sight of the male.
Males perform signal jumps and dips also beyond the
spawning season (Kenyon, 1994; Mann and Lobel,
1995, 1998; Picciulin et al., 2002). It is recorded that
at territorial contacts or conflicts, peculiar acoustic
dialogues can take place between the participants of
KASUMYAN
40 60 80
Time, ms
such relationships. For instance, when Q. meleagris
penetrates to the territory protected by male D. albi
sella, not only short and abrupt pops sounds emitted
by the owner of the territory are heard, but also
response sounds similar to a buzz emitted by an
intruder (Mann and Lobel, 1998).
High aggressiveness is typical also of still another
Pomacentridae—A. luridus. They furiously attack any
fish that approach the boundaries of their territory—
other males of their species and fish of other species
(wrasse Thalassoma pavo, salpo Sarpa salpo, small
mouthed wrasse Centrolabrus trutta, sharpnosed puff
erfish Canthigaster rostrata, and gray mullets Mugil
spp.). In most cases, males of A. luridus emit sounds of
aggression at the moment of darting at an intruder.
When male A. luridus beats, bites, or pursues the
escaping enemy, it does not emit sounds. Sound emis
sion is accompanied by a typical zigzagshaped swim
ming of the male. Sounds arise also in the absence of
an actual enemy when male A. luridus patrols the ter
ritory protected by it whose sizes are usually small
(radius approximately 1 m). In females and immature
males of A. luridus, no sound generation was revealed.
Male sounds represent small series consisting of two to
five double (paired) pulses where the second pulse is
always stronger than the first pulse (Fig. 12). The basic
sound frequency averages 400 Hz with harmonics up
to 2500 Hz; sound duration is approximately 2–3 s.
The presence of harmonics indicates the drumming
mechanism of sound generation, although no tym
panic muscles in Pomacentridae fish were found.
Sounds emitted by male A. luridus in nature or under
artificial conditions at an intraspecies aggression or at
attacks of fish of other species that swim up to the ter
ritory have similar acoustic parameters (Santiago and
Castro, 1997). Males of another species of Pomacen
tridae, green damselfish A. abdominalis, emit sounds
of aggression constantly—when they patrol their site,
clean substrate for the nest, and even when try to
attract a female to the nest. Sounds are often heard
during a dart on the enemy (individuals of the own
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
species, different species of Labridae, Chaetodon
tidae, Scaridae, Acanthuridae, etc.) and during its
pursuit (Fig. 2). Sounds of aggression in
A. abdominalis represent either one to two short pulses
or series with a duration of approximately 1000 ms
consisting, on average, of five pulses. The dominant
frequency of such sounds is in the range of 120–
250 Hz. Producing these sounds, males widely spread
all their fins (Maruska et al., 2007).
Males of another Pomacentridae, blue damselfish
L. chromis, that protect their sites emit abrupt and very
short single clicks or pops with a frequency of 250–320 Hz
(Picciulin et al., 2002). Another closely related spe
cies, C. viridis, during agonistic manifestations (pur
suit of the enemy) emits a series, on average, of
12 pops with a dominant frequency of approximately
700 Hz (Amorim, 1996). Sounds of the type of pops
are emitted by Plectoglyphididon lacrymatus at the
manifestation of territorial aggression with respect
even to a man approaching the aquarium. A fish that
protects its territory orients at an intruder, widely
spreads pectoral fins, and emits pops that represent
series of two to five individual acoustic pulses with a
duration of 50–60 ms followed by intervals of 180 ms.
Sound frequency embraces a range of 100 to 1000 Hz
with maximum amplitude at 330 Hz. The duration of
such pops varies from 200 to 700 ms. During manifes
tation of agonistic behavior, pops are emitted by Das
cyllus aruanus living together with P. lacrymatus; how
ever, its sounds have other acoustic parameters (Par
mentier et al., 2006). Pops, chirps, or clicks are
emitted by many species of Amphiprion also belonging
to the family Pomacentridae (Schneider, 1964b; Chen
and Mok, 1988).
The emission of warning acoustic signals for pro
tection of its own site is typical of fish of many taxo
nomic groups. Such sounds are emitted, for instance,
by Gobius cruentatus from Gobiidae (Rocca et al.,
2001), Halichoeres bivittatus from Labridae (Steinberg
et al., 1965), and Sebasticus marmoratus from Scor
paenidae (Miyagawa and Takemura, 1986). Sounds of
males of Cyprinodon variegates (Cyprinodontidae), in
most cases, are heard during patrolling of the territory;
less frequently, when a male stays in the center of its
site, when it pursues the enemy, courts a female, or
during spawning (Nicoletto and Linscomb, 2008).
The territorial males of Cyprinodon bifasciatus emit
short (50–60 ms) monopulse sounds during pursuit of
males of their own species or of other fish (Cichlasoma
minckleyi) that approached them (Johnson, 2000).
Zander Stizostedion lucioperca (Percidae) vehe
mently protects its nest: at the approach of an enemy,
it assumes a threatening posture (spreads dorsal fin,
widely opens operculi), emits strong percussive
sounds, and attacks the enemy (Protasov and
Nikol’skii, 1969). Males of round goby N. melanosto
mus (Gobiidae) are no less aggressive. Protecting their
nest, they, spreading unpaired fins and widely opening
operculi, fearlessly attack the approaching crabs, fish,
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
983
such as atherine Atherina mohon pontica or zander, and
even the observing scuba diver. Simultaneously, the
male emits husky abrupt sounds that resemble growl
with duration approximately 1.5 s and a frequency of
approximately 200 Hz (Protasov et al., 1965). Warning
sounds are emitted by Padogobius martensii when they
attack or pursue intruders (Torricelli and Romani,
1986).
For a male of Atlantic cod when it is kept under
artificial conditions, it is sufficient to emit typical
grunts to frighten an undesirable intruder that
appeared at the protected territory. Usually the resi
dent emits such a sound when the distance between it
and the fish that penetrated to its territory decreases to
10–15 cm and even more. For fish located at a dis
tance of 60–80 cm and over, resident’s sounds are
indifferent (Brawn, 1961b). Grunts at agonistic inter
actions with other males or with females of the same
species that are not ready for spawning, or with fish of
other species are also emitted by males of other
Gadidae—haddock, walleye pollack, and lythe
(Hawkins and Rasmussen, 1978). Placing of an addi
tional male to a spawning pair of haddock in the basin
leads to a significant increase of sound duration, which
can be caused by competition between the males
(Bremner et al., 2002).
In Cichlasoma centrarchus (Cichlidae), in the
spawning period, sounds of males suppress the aggres
sivenes of other males and decrease in them the desire
to penetrate to the occupied sites and come into con
flict relations with the hosts of the territory. In C. cen
trarchus, the sounds of aggression are emitted by males
and females; the intensity of sound generation in them
is directly related to aggressiveness: prior to deposition
of eggs, males that at this time actively protect their
own territory and establish dominance over the female
vocalize most intensively. Females intensify sound
generation after spawning when their increasing
aggressiveness is related to protection of the offspring
(Schwartz, 1974). In another Cichlidae, Mozambique
tilapia Oreochromis mossambicus, in the beginning of
the period of formation of intraspecies hierarchy when
the number of symmetrical aggressive contacts
(encounters in which an attacked male responds to an
enemy by active actions) decreases and the number of
asymmetrical contacts increases, sounds are absent. At
this time, all aggressive contacts and interactions
related to the assessment by enemies of each other and
the choice of the territory are produced by silent
males. The first sounds are recorded only after a dom
inant territorial male that changed its coloration from
usual to black and is actively engaged in nest construc
tion and then its protection appears among fish.
Sounds are more frequently associated with elements
of behavior of the dominant male such as staying still
on the bottom of the nest with pressed unpaired fins
(usually after actions for deepening of the nest and cir
cling above it), slight tail wagging, and taking of an
inclined posture. The sounds have two maxima at 38
984
Fig. 13. Acoustic signaling in bullhead Cottus gobio at aggressive interactions: the left male attacking an invader emits growls, it is
more intensively pigmented, its operculi are widely set apart; the oscillogram shows a series of five pulses, the length of the hori
zontal fragment corresponds to 50 ms (Ladich and Myrberg, 2006).
and 350 Hz; sound duration varies from 0.1 to almost
3.0 s, on average, approximately 0.7 s (Amorim et al.,
2003). Sound parameters in males of Mozambique
tilapia change after interaction with other males.
Immediately after a fight, a winning male not only
more rapidly starts to court a female and more inten
sively and for a longer period courts it, but also emits
more frequently sounds in which pulses are more pro
longed, and the dominant frequency is lower than in
males that not long before have suffered defeat in the
fight. It is assumed that these changes are caused by
shifts in the concentration of monoamines and corti
sol in the fish body after stress induced by an unsuc
cessful fight (Amorim and Almada, 2005). The mech
anism of sound generation in Mozambique tilapia
changes after interactions with other males. It is sug
gested that sounds in these fish arise at rubbing of the
pharyngeal teeth (Lobel, 2001).
Sounds in the reproduction period are emitted by
males of some Cyprinidae that pass at this time to the
territorial mode of life. For instance, males of Codoma
ornate in the aquarium occupy suitable shelters
between large objects and drive away other males that
approach them. The most aggressive contacts between
males are expressed in lateral demonstrations, close
circlings around each other, and mutual pursuits.
When an aggressively tuned male approaches the
occupied site, the owner emits a warning acoustic sig
nal—a relatively lowfrequency nonharmonic sound
that resembles a burst. During aggressive interactions,
male coloration changes from monotonously gray to
black with silvery marks at operculi. Males assume the
same coloration during courtship of the female
expressed in swimming before the entrance to the
crevice shelter and during its own spawning when
sounds of the burst type are heard. The mechanism of
generation of these sounds is unknown. Females pro
duce no sounds (Johnston and Vives, 2003). A similar
mode of behavior is observed in males of another
North American Cyprinidae, Pimephales notatus,
which, in the reproduction period, also protect their
own sites and display care of the offspring. Sounds are
KASUMYAN
produced only by spawning males, mainly during ago
nistic contacts with other males. In the repertoire of
males, there are four nonharmonic sounds differing in
duration, periodicity of generation, and frequency
that in these small fish (approximately 10 cm) is
extremely low, on average, 60 to 80 Hz (C. Johnston
and D. Johnston, 2000b).
The role of sounds in the territorial behavior of fish
beyond the reproduction period. Sounds related to the
territorial behavior are emitted by many fish protect
ing their sites also beyond the reproduction period.
Throughout the year, agonistic acoustic signals are
generated by river bullhead Cottus gobio (Cottidae),
both males and females. The acoustic repertoire of
these fish consists of two types of sounds—knocks,
single or produced in series, and growls. More fre
quently, the bullhead emits single knocks (in more
than 90% of cases) with a duration of 48 ms and a wide
band of the dominant frequency (50 to 500 Hz).
Sounds are generated when one of bullheads notices
the approach of another, when it exhibits threat, or
pursues the enemy, but not at the moment of a direct
encounter and struggle. In the case of threat, bullhead
draws aside its operculi and the gill membrane, opens
and protrudes mouth, lowers its head to the ground,
makes nods, intensifies pigmentation, and emits
sounds. In its enemy, these sounds can cause a
response demonstration of a threat and approaching
their source (Fig. 13) (Ladich, 1989). Similar behav
ior, in particular touchings and thrusts or blows with
head or body against the ground are typical also of
other Cottidae at antagonistic contacts and attracting
a female by the male for Cottus bairdi, Myoxocephalus
octodecimspinosus, Paracottus kneiri, and Cottocome
phorus grewinki (Barber and Mowbray, 1956; Dmit
rieva and Ostroumov, 1992; Whang and Jansen, 1994).
Blows with the head and slaps with the body against
the ground in C. bairdi are rather intensive and raise a
cloud of suspension to water. Sounds arising in this
way resemble single knocks and less frequently a series
of two or more knocks. Sound frequency is low (32–
105 Hz) (Whang and Janssen, 1994). As a result of
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
such actions, acoustic oscillations arise that in the sub
strate damp far more slowly than in water. Sounds gen
erated by fish lying on the bottom using special organs
also can penetrate and distribute in the bottom sub
strate. Such mode of acoustic signaling via ground can
be very efficient and important for communication of
bottom fish, especially with a twilight or nocturnal
type of activity.
Acoustic signaling beyond the reproduction period
is likely typical of the territorial behavior of many fish,
especially those that are components of multispecies
communities in bottom or physically complexstruc
tured biotopes, such as, for instance, coral reefs. Such
wellstudied fish include, for instance, butterfly fish of
the genus Chaetodon (Chaetodontidae) that have
developed accessory auditory structures, which per
mits assigning these fish to acoustic specialists (Webb,
1998; Webb and Smith, 2000; Webb et al., 2006). But
terfly fish are characterized by a complex social behav
ior related to their monogamy and defense of relatively
large own sites where the pair protecting them feeds
and reproduces and where it can constantly stay dur
ing many years (Roberts and Ormond, 1992). It was
long considered that the capability for sound genera
tion is lacking in these fish. However, observations and
interesting experiments performed directly in nature
demonstrated that the territorial behavior of Chaet
odon is accompanied by the generation of diverse
sounds addressed for conspecific intruders and for a
partner over the territory. A transparent plastic bottle
with another fish of this species placed into the center
of the site (50–100 m2) protected by the pair of C. mul
ticinctus as soon as after 10 s is detected by the hosts of
the territory and is attacked. Sounds are heard most
frequently when after several lateral demonstrations
the butterfly fish slowly moves to the intruder, and then
turns around and makes a sharp blow with a caudal fin
(Fig. 14). Such blow lasts less than 200 ms and causes
a prolonged and lowfrequency hydrodynamic pulse
(150 ms, 50–110 Hz) and a short highfrequency click
(10 ms, 3400 Hz). The host of the territory can swim
up to the intruder, and they can exchange typical
movements of ventral fins—their rapid upward move
ments and slow downward movements. Both fish at
this time emit short (17 ms) sounds with a frequency of
approximately 230 Hz. Considerably less frequently
one can observe typical jumps of the host when it
directly approaches the bottle with the intruder in it,
then abruptly turns round by 180°, moves away along
the inclined line upwards by 0.5 m, and begins inten
sive lateral demonstrations—swimming with partially
spread fins by its side to the intruder, turning away
from it to the side. At this moment, a series of several
short sounds is heard. When there is a pair of intruder
fish in the bottle, typical grunt sound representing a
series of individual pulses following each other with a
periodicity of 3 pulses per second are often recorded.
This sound has a basic frequency of 163 Hz and several
harmonics. The duration of such grunts averages 6 s;
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11
985
4
3 1
2
(a) (b)
(c) (d)
Fig. 14. The behavior of butterfly fish Chaetodon multicinc
tus: (a) a slow approach of the host of the territory to an
unknown invader fish, an abrupt turn round, and a sharp
strokeslap with a caudal fin; (b) (1) a slow approach of the
host of the territory and examination of an unknown fish,
(2) a rapid turn round by 180°, (3) moving upwards along
the inclined line and (4) lateral displays; (c) reciprocal
exchange of the host of the territory and the unknown fish
with typical visual demonstrations—rapid upward move
ments and slow downward movements of ventral fins;
(d) generation by one of unknown invaders of a warning
sound that the hosts of the territory have appeared (Tricas
et al., 2006).
such sound is generated by one of the fish; it arises
when the hosts appear at a distance of 3 m and is inter
preted as a warning signal for a partner about the dan
ger that arose (Tricas et al., 2006).
Sounds—clicks and knocks are emitted by imma
ture Botia modesta (Cobitididae). Prolonged warning
clicks are heard when the physical contact between the
interacting fish is absent—during the approach of a
competitor, at lateral demonstrations, and circlings.
More rapid and loud knock sounds arise during cir
cling when one of the fish pushes by its head the tail of
another. Both sounds are so strong, that are easily
heard by a man who is several meters away from the
aquarium. During pursuit, fish generate no sounds
(Raffinger and Ladich, 2000). Acoustic generation
accompanies aggression in Trichopsis (Osphronemi
dae). Croaking gourami T. vittata begins to emit
sounds immediately after the removal of a partition
isolating one male from another, and the enemies
begin to demonstrate reciprocal threats (lateral and
frontal demonstrations), circle round each other, per
form short fights or prolonged combats, and pursue
the running away fish (Fig. 15). Sounds of croaking
gourami can be heard even at a distance from the
aquarium with fish. Sounds are emitted by both males
and females, their sounds are similar. The mechanism
2009
986 KASUMYAN

(a)

(b)

(c)

Fig. 15. Aggressive behavior of croaking gourami Trichopsis vittatus accompanied by sound emission: (a) frontal demonstration,
(b) combat (both enemies produce sounds), and (c) pursuit. During frontal demonstrations and combat, in both enemies, hori
zontal black stripes are well seen on the body and head; during pursuit, the coloration of the winning male is light and black stripes
disappear (a and c) according to Henglmüller and Ladich, 1999; (b), according to Ladich, 2004).

of sound generation in croaking gourami is stringed,
proper sounds represent series of double pulses arising
in time with movements of pectoral fins. Individuals
that were artificially devoid of a capability to produce
sounds become winners in combats less frequently
than intact fish of similar sizes (Ladich et al.,1992a,
1992b; Wysocki and Ladich, 2001). This example
stresses the importance of threat sounds in the aggres
sive behavior of fish and formation in them of intra
group hierarchy. It is of interest that the aggressive
behavior and vocalization in different representatives
of this genus differ. For instance, frontal demonstra
tions are typical only of croaking gourami; a strong
beating with a caudal fin simultaneously with vocaliza
tion, the greatest distance between the circling ene
mies, and a small number of attacks are typical for
T. pumila; the greatest duration of fights, number of
circlings, and emitted sounds are typical for T. schal
leri (Bischof, 1996). Weak and rare sounds during
fights are emitted by closely related to Trichopsis
Macropodus opercularis and Colisa lalia (Osphronemi
dae) (Bischof, 1996).
In Gaidropsarus mediterraneus, sounds resembling
dull knocks arise in a situation when a fish smaller in
size that accidentally approached or penetrated into
the occupied shelter is attacked by a larger host that
vehemently attacks the intruder, seizes it, and keeps it
with its jaws within several seconds, pursues, and
drives it out. Sounds have an average duration of
approximately 80 ms and a frequency of 50 to 750 Hz
with maximum amplitude at 150 Hz. Tympanic mus
cles in G. mediterraneus, unlike other vocalizing
Gadidae were not found; therefore, the mechanism of
sound generation remains unclear. It is also unclear
which of the two fish, resident or the invader, emits
sounds, i.e., whether they are threat sounds or imita
tion sounds (Almada et al., 1996).
Sound generation accompanies aggression in
Micropterus coosae (Centrarchidae) caused by placing
into the aquarium to a single individual of another fish

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

 ACOUSTIC SIGNALING IN FISH
Table 6. Frequency of production and acoustic characteristics of sounds emitted by males of Codoma ornate at different mani
festations of aggressive and reproductive behavior (Johnston and Vives, 2003)
Frequency of sound
Behavior Sound duration, s
production, %
Pursuit of an enemy 11
Lateral demonstrations 57
Circling 99
Courting a female 78
Spawning 100
of the same species. Sounds are recorded during pur
suit of the enemy by the resident, pushes and knocks,
lateral demonstrations and circlings, as well as after a
fight, as is assumed, by the winner when enemies
depart and freeze. Sounds are emitted by both males
and females of M. coosae. The dominant frequency of
the sound is approximately 170 Hz, average sound
duration is 1.25 s, and it can include 1 to 41 pulses
(Johnston et al., 2008). During aggressive interac
tions, sounds are emitted by Silurus glanis (Silu
ridae)—short signals with an average frequency of
300 Hz, duration of 35 ms, intervals of 2–6 s, and an
instant increase in the amplitude (Sorokin and Sima
kov, 2004). The territorial males of Chasmodes bosqui
anus emit sounds (Tavolga, 1958a).
Comparison of spawning sounds and sounds of the
territorial behavior. In the reproduction period,
sounds related to the manifestation of aggression or
competition for the territory are generated almost
simultaneously with spawning sounds. These sounds
in some species can differ and in other species can be
similar. For instance, males of bicolor damselfish
capable of emitting diverse sounds generate the same
sound resembling chirps both in the early morning
hours when they court a female and spawning occurs
and throughout the remaining part of the day when
males are engaged in exclusively the protection of their
own nest (Myrberg and Riggio, 1985; Myrberg, 1997).
In other fish, males protecting their nest sites use some
sounds to attract a female and other sounds, as warn
ing signals. In plainfin midshipman, large territorial
males for attracting a female emit prolonged monoto
nous hums, and during agonistic contacts, short grunts
or more prolonged grunts and growls (Fig. 4) (Brant
ley and Bass, 1994; Bass et al., 1999). Warning grunts
are emitted also by oyster toadfish O. tau. Unlike loud
inviting boatwhistle sounds generated by males, grunts
are produced by both males and females of oyster
toadfish.
Shorter grunts have a wider frequency band and are
intended, as is considered, for regulation of agonistic
contacts between individuals of both sexes (Gray and
Winn, 1961; Fish and Mowbray, 1970; Fine et al.,
1977a). Grunts in oyster toadfish are of several types;
they arise throughout the year; however, grunts are
most frequently heard during the reproduction period
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11
987
Dominant Subdominant
frequency, Hz frequency, Hz
0.55 60 191
2.79 84 173
7.77 54 157
6.60 62 251
4.93 82 209
(Maruska and Mensinger, 2009). Sounds for attraction
of females in oyster toadfish and plainfin midshipman
are emitted only by males and only in the reproduction
period when warning sounds are heard during all sea
sons; they can be generated by males and females and
not only in connection with agonistic contacts, but
also during fright and stress, for instance, at handling.
These sounds are characterized by a low variability of
the basic acoustic characteristics (Table 1) (Fine,
1978; Bass, 1990, 1996; Barimo and Fine, 1998). Cyp
rinid fish Codoma ornate at aggression, during courting
a female, and during spawning emits burst sounds dif
fering in their acoustic characteristics (Table 6)
(Johnston and Vives, 2003).
Thus, the spawning and territorial behavior can be
regulated in some fish using different sounds, and in
other fish, the same sound can be used in different
behavioral situations. It is likely that this is determined
by the fact of how well developed is the soundgener
ating apparatus, how specialized is acoustic signaling,
and how well developed are forms of communication
in fish of a particular species. For instance, in male
Atlantic cod, sounds intended for a mature female are
similar to sounds of aggression generated by it during
penetration to its territory of another male. In had
dock having a far more diverse spectrum of sounds,
agonistic sounds and sounds that arise in interactions
with females differ: the former represent series of slow
knocks and the latter represent a series of substantially
rapid knocks (Brawn, 1961b; Hawkins and Amorim,
2000).
During agonistic or aggressive manifestations, not
all fish emit sounds. Pseudorasbora parva (Cyprin
idae), when two individuals are placed together, usu
ally demonstrates pursuits, circlings, and beats with a
tail; however, no sounds at this time were recorded
(Scholz and Ladich, 2006). Sounds initially indiffer
ent for fish can assume a signal importance owing to
training when their presentation is combined with the
action of the unconditioned stimulus. In Pimephales
promelas (Cyprinidae) and Hemigrammus erythrozonus
(Characidae), such reflex is formed immediately after
a single presentation to fish of an inert acoustic stimu
lus together with a threat pheromone—a natural
chemical signal of danger present in the fish skin
(Wiseden et al., 2008).
2009
988 KASUMYAN

(a)
Time, ms
250 500 750 1000 1250 1500 1750

Amplitude
Amplitude
Frequency, Hz

600
400
200
25 50 75 100
Time, ms
(b)
Time, ms
250 500 750 1000 1250 1500
Amplitude
Amplitude
Frequency, Hz

600
400
200
50 100 150
Time, ms

Fig. 16. Oscillogram, its separate fragment, and a sonogram of sounds of the type of (a) “bark” and (b) “growl,” corresponding
to this site emitted by John dory Zeus faber at a strong stress (Omiki and Somiya, 2004).

Available published data allow to conclude that
sound generation is a typical feature of biology of
many typical territorial fish that spend most part of
their life at their own sites and defend them from com
petitors. The owner of the territory generates sounds
for signaling that the site is occupied, emits warning
sounds when it notices other approaching fish, or
threatens them, and can emit sounds during attack,
fight, or pursuit of aliens. The emission of such sounds
helps fish to maintain rights for the own site, which is
especially important in the reproduction period since
many fish not only deposit eggs here but also guard
them and the juveniles that emerged. The use of
acoustic signaling for defense of own sites is typical
first of all of males, but in several fish different in tax
onomy, females also possess this capability, for
instance, Dascyllus abdisella (Pomacentridae),
Cichlasoma centrarchus (Cichlidae), Cottus gobio
(Cottidae), Trichopsis vittata (Osphronemidae), and
Micropterus coosae (Centrarchidae). The generation
of sounds of aggression in female fish occurs mainly
beyond the reproduction period.
Defensive Behavior
Many fish are characterized by sound production
during manifestation of protective (defensive) behav
ior in response to stimuli causing in fish fright or
stress—mechanical impacts, shocks with an electric
current, handling, the appearance of a predator or sig
nals imitating its presence, etc. The study of sounds
arising namely in stress situations dominated in early
papers on fish bioacoustics (Dufossè, 1874; Fish et al.,
1952; Fish, 1954; Tavolga, 1971; Myrberg, 1981).

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

 ACOUSTIC SIGNALING IN FISH
At fright, when fish for a short time are taken out of
water, males and females of swanky sweeper Pempheris
schwenkii emit sounds—a series of 2–7 pulses, with a
duration of 56 ms, dominant frequency of 100 Hz, and
two harmonics (Takayama et al., 2003). In the same
situation, sounds are emitted by John dory Zeus faber,
more frequently a sound of the type of barks and much
more seldom a second sound resembling growls. These
sounds differ in amplitude, duration, and frequency:
barks are a sequence of 4–14 pulses; grunts consist of
one pulse of the same duration (Fig. 16). Distinct ideas
of the importance of these sounds in the behavior of
John dory are absent up to now (Onuki and Somiya,
2004). Typical hum is emitted by Myoxocephalus scor
pius caught by line fishing and raised above water (per
sonal obsevations) that, as Russian naturalist
N. Zograf writes in his remarkable survey Music of
Aquatic Inhabitants (1890), in Russia the White Sea
fishermen called “revets” or “ryavtcha” (grunter,
croaker), and in Germany, the residents of the Baltic
coast called it a “grunting cock” (Knurrhahn). Zograf
cites also own observations of Cottus gobio, closely
related to M. scorpius, that at stress (in air) also pro
duces a sound resembling blows of a hammer upon a
wooden plate and corresponding to the C flat note of
the piano.
The emission of a grunt sound at fright caused by
retaining fish in a landing net in the air is typical of
males and females of oyster toadfish O. tau. Grunts at
fright are more prolonged and have higher frequency
than grunts emitted by oyster toadfish at agonistic
contacts (Barino and Fine, 1998; Maruska and Mens
inger, 2009). At fright when taken out from water, pep
pered corydoras Corydoras paleatus emits sounds;
these sounds generated owing to the functioning of
pectoral fins differ from those emitted by males of
C. paleatus during courting a female in the reproduc
tion period. Fright sounds consist of a simple sound
that arises at the flap with one of the pectoral fins and
differs from spawning sounds representing a series of
several simple sounds. The greater relative sizes of the
first ray of the pectoral fin, the more prolonged sound
that in males lasts on average for approximately 20 ms,
in females lasts approximately 16 ms, and in immature
fish lasts approximately 13.5 ms. Sounds at fright are
generated by males, females, and immature individu
als, while during spawning only males vocalize
(Pruzsinszky and Ladich, 1998). The emission of
stridulation sounds at fright is typical also of other rep
resentatives of Siluriformes (Ladich, 1997), for
instance, for Pseudobogrus fulvidraco.
Stress induced by transfer to another aquarium is
accompanied in Sygnathidae by the generation of typ
ical for them clicks (Fish and Mowbray, 1970).
A serious stress factor for fish is an unexpected
appearance of a large predator. In such a situation,
sharp sounds resembling grunts are emitted by Trigla
lucerna (Triglidae). The sound generation is accompa
nied by visual signaling—raising of dorsal fin and
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
989
spreading large and brightly colored pectoral fins. All
this, as is assumed, is directed to frighten off the pred
ator, as well as to induce anxiety and a similar response
in other fish also. Northern searobin Prionotus caroli
nus emits sounds and exhibits anxiety in a similar way.
It is assumed that such behavior in these fish can be
related also to intragroup relations (Fish, 1954; Fish
and Mowbray, 1970; Connaughton, 2004). At an
encounter with a predator such as conger Conger con
ger, Atlantic cod emits grunt sounds. The same sounds
arise in the cod at a fright caused by the attack of a ter
ritorial male (Brawn, 1961b). In response to a strong
stress from an encounter with predatory marine mam
mals, cod can emit clicks, louder and higherfre
quency (4–8 kHz) sounds than grunts (Vester et al.,
2004). Short and abrupt sounds (staccato) and grunts
are emitted by Holocentrus rufus at the sight of a pred
ator or its approach (Winn et al., 1964). Polypterus ret
ropinnis emits a sound of the type of moans when it is
frightened or rapidly swims away after an unexpected
encounter with another representative of its species
(Ladich and Tadler, 1988).
Single grunts at stress are produced by plainfin
midshipman (Brantley and Bass, 1994; Bass, 1996).
Sounds resembling a squeak or croak are emitted by
Gobio gobio at excitation and at fright, as well as in
response to touchings or pushes of an individual swim
ming close by or at a rapid approach to another gud
geon resting on the bottom. No obvious responses in
partners of a gudgeon school were observed except a
shorttime one, for several seconds, cessation by the
remaining fish of foraging in the ground (Ladich,
1988).
Sounds that arise at fright or at appearance of an
actual danger are usually short and abrupt, which sug
gests that they are used as warning or frightening off
signals. However, there are no direct experimental
proofs of such suggestion. In fish with a limited acous
tic repertoire, the same sounds can be used apparently
in different situations, as, for instance, in males of gray
weakfish C. regalis that at stress when they are taken
out of water emit short drumming sounds of anxiety
resembling sounds generated by males in the repro
duction period (Connaughton et al., 2000). However,
in peppered corydoras C. paleatus, spawning sounds
and stress sounds differ (Pruzsinszky and Ladich,
1998).
The defensive behavior can be not only accompa
nied by sound emission, but also caused by sounds
whose source can be not only proper fish, but also
other aquatic inhabitants. For instance, Clupeidae of
the genus Alosa are characterized by a defensive
response to ultrasounds (80–150 kHz) that are pro
duced by predatory Cetacea at determining the loca
tion of prey (Dunning et al., 1992; Nestler et al.,
1992). Acoustic oscillations with a frequency to 10 Hz
arising during swimming of large predatory fish can
also serve as repellent signals for potential prey (Enger
et al., 1989).
990 KASUMYAN
Group and Aggregative Behavior
There are extremely few data indicating the use by
fish of sounds for the regulation of intragroup relations
or intragroup contacts. It is known that in Carapus
possessing a welldeveloped sound generating drum
ming apparatus, sound emission is observed only dur
ing penetration of fish into the host holothurian, in
which several individuals of the same species are
already present. At approach to the holothurian in
which there are no fish, or immediately before pene
tration into it, Carapus do not emit sounds. Nor do
they emit sounds when they are located within a
holothurian (Parmentier et al., 2003). Undoubtedly,
sounds produced by Carapus in the case when they
approach a holothurian in which there are other Car
apus may be related to social behavior. However, how
Carapus manage to determine the presence in a
holothurian of other Carapus not emitting sounds
remains unclear. The importance of acoustic signals
emitted by Carapus before entering a holothurian with
fish that are already in it is also not quite clear. Possibly,
such signals in some way affect the behavior of fish sit
ting in the holothurian and prepare them for the
appearance of a new neighbor.
Sounds, as is assumed, can serve as signals of obe
dience of small fish with a low hierarchical rank and be
addressed to larger and stronger partners in the group.
Such signaling exists apparently in Ictalurus nebulosus
(Rigley and Muir, 1979, cited from Fine et al., 1996).
Sound generation is typical of Polypterus (Polyp
teridae) distinguished by high aggressiveness, but
manifesting no obvious signs of territoriality. When
two different species of these fish, P. retropinnis and
P. senegalus are kept in common in one aquarium,
thumps are heard only at an encounter with conspe
cific fish; the rate of sound emission reaches maxi
mum (up to three sounds per second) at the closest
contact of individuals and drastically decreases after
they move from each other (Ladich and Tadler, 1988).
Some aggregative fish, such as gudgeon, emit spe
cialized sounds whose main purpose, as is assumed, is
related to maintaining a certain distance between indi
viduals, which is especially important in feeding of
these fish. Gudgeon emits sounds only when several
individuals are kept together, when they move over the
aquarium in a school, mainly for foraging (digging or
burrowing in the bottom ground). No sounds are reg
istered in fish placed separately (Ladich, 1988). It is
assumed that social contacts in herrings, Atlantic cod
Clupea harengus and Pacific cod C. palassi, can be
maintained using pneumatic sounds. Herrings pro
duce these sounds mainly during dark hours of the day
when there is no possibility of visual signaling. Sound
generation increases at a denser fish stock (Wahlberg
and Westerberg, 2003; Wilson et al., 2004). Unspecial
ized hydrodynamic sounds produced by swimming
fish schools, especially at the moment of a drastic
increase in the swimming rate or at unexpected and
JOURNAL OF ICHTHYOLOGY
rapid maneuvers, are unlikely to help fish to retain the
school or synchronize movements of particular indi
viduals. However, it is possible that typical lowfre
quency nonharmonic sounds of a swimming school
can serve as landmarks for fish that became separated
from the school and facilitate their return to the
school.
Feeding Behavior
Feeding process when fish seize the discovered prey
and subject it to intraoral processing is inevitably
accompanied by sounds that are often called feeding
sounds. These sounds are common during acoustic
monitoring of natural water bodies (Anderson et al.,
2008). An increase of the acoustic background
observed in water bodies with the onset of evening twi
light is related namely to such fish sounds (Protasov,
1965). These sounds in the majority of cases are
unspecialized; they arise involuntarily and accompany
food seizing and processing.
In large ichthyophage fish (pike Esox lucius, zander
S. lucioperca, snakehead Ophiocephalus argus, etc.),
grasping of fish is accompanied by a typical pop or
knock; during feeding of different small fish, smacks,
clatter, and knocks are heard. Sounds of bursts or rub
bing arise during chewing of food (Protasov and
Romanenko, 1962). Two sound categories, bursts and
pops, are recorded during feeding of coastal marine
tropical fish Haemulon album (HaemulidaePoma
dasydae). A sound resembling bursts is heard during
feeding of these fish from the bottom when together
with food, substrate is also seized, then it is subse
quently ground and removed through gill openings.
Sounds similar to pops arise during seizing plankton
prey (Cummings et al., 1964). Clicks with the domi
nant frequency of 400–800 Hz are emitted by feeding
lined seahorses Hyppocampus (Fish and Mowbray,
1970; James and Heck, 1994; Bergert and Wainwright,
1997; Colson et al., 1998). Sounds accompanying
feeding are described for Halichoeres bivittatus and
Labrus viridis (Shishkova, 1958; Steinberg et al.,
1965), in carp Cyprinus carpio, and minnow Phoxinus
phoxinus (Stepanek, 1968), in rainbow trout Onco
rhynchus mykiss (Phillips, 1989; Lagardère et al.,
2004), and in Tramitichromis intermedius (Lobel,
2001). In carp, minnow, T. intermedius, and Scoph
thalmus maximus, these sounds are relatively short,
approximately 75, 25, 9, and 5 ms, respectively, while
in rainbow trout, they reach a duration of 1000 ms
(Stepanek, 1968; Phillips, 1989; Lagardère and
Mallekh, 2000; Lobel, 2001; Lagardère et al., 2004).
In the experiment, responses to isolated presentation
to fish of recordings of such sounds is observed rarely,
which, as is assumed, is related to the absence of an
additional stimulation along other sensory canals
(Scholz and Ladich, 2006). It is noted that rainbow
trout responds to feeding sounds only in the presence
of a visual contact with other feeding fish (Phillips,
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH 991

AmplitudeFrequency, kHz
1989). In many fish, a conditioned reflex to unspecial
ized feeding sounds is easily formed. These sounds (a)
cause an orientation response or attraction of fish to 1
their source. The intensity of response to a sound dras
tically increases at the combination of feeding sounds
with the visual or odor stimulation (Protasov and
Romanenko, 1962).
Sounds emitted by fish during feeding differ. When
stone moroko Pseudorasbora parva is fed on oligocha
etes Tubifex sp. or larval mites Chironomidae, rather 50 100 150
prolonged chewing sounds are heard; they are absent Time, ms
when fish are fed on flakes of artificial feed. When

Amplitude Frequency, kHz

stone moroko is fed on any of these feeds, feeding
strike sounds are well heard; these sounds are three (b)
times shorter when fish consume natural food. In all 1
cases, feeding sounds have a wide frequency range
with maximum amplitudes in the zone of 100 to
800 Hz; the most audible sounds are sounds of grasp
ing by fish of flukes of artificial feed (even with a naked
ear) (Scholz and Ladich, 2006). There is a hypothesis
that high auditory sensitivity inherent to socalled
auditory specialists, in particular, to Cyprinidae and
other Ostariophysi, is an adaptation allowing these 50 100 150
fish, in many of which no acoustic communication Time, ms
was found, to perceive sounds produced by other fish (c)
and aquatic animals, including feeding sounds (Scholz
2
and Ladich, 2006).
Frequency, kHz

There are few known specialized sounds produced

by fish purposefully for regulation of feeding behavior;
1
they are studied comprehensively only with respect to
gurnards, streakedgurnard Trigloporus lastoviza, and
gray gurnard Eutrigla gurnandus—bottom coastal fish
inhabiting depths of 20 to 160 m in the Mediterranean
Sea and in the Eastern Atlantic. These fish lead a non
Amplitude

territorial group mode of life and feed in common at

the same site. As in other representatives of the family
Triglidae, in streaked gurnard and gray gurnard there is
a large swimming bladder and well developed tym
panic muscles. Acoustic signaling in Triglidae is
directed at a decrease in the food competition between
individuals feeding in common when they are forced
to compete between themselves for a limited amount
of food (concurrent feeding). In the experiment when
fish are kept in the same basin, T. lastoviza produce
clearly heard sounds that resemble growls, grunt, or
rumble. The frequency of these sounds does not
exceed 2000 Hz; maximum amplitude of oscillations
is, on average, in the range of 600–700 Hz. Each sep
arate sound continues, on average, for approximately
3 s and consists of a series of groups of 1–3 pulses fol
lowing with a certain interval (on average, 37 groups of
pulses in a sound). The acoustic repertoire of E. gur
nardus is far richer; it consists not only of sounds of the
type of growls, but also of sounds resembling grunts
and knocks. All these sounds represent series of groups
of short and lowfrequency acoustic pulses differing
between themselves in the number of groups in a series
and, correspondingly, in sound duration (Fig. 17).
Knocks are the least prolonged (12 ms) and usually
50 100 150
Time, ms
Fig. 17. Sonograms (on the top) and oscillograms (below)
of sounds emitted by Eutrigla gurnardus at concurrent
feeding: (a) knocks, (b) grunts, and (c) growls (Amorim
et al., 2004b).
consist of 1–2 groups of pulses. Sounds of the type of
grunts are prolonged (approximately 70 ms) and rep
resent series, on average, of six groups of pulses.
Sounds of the type of growls in E. gurnardus are the
most prolonged; their average duration is 264 ms
(40 groups of pulses), which, however, is ten times less
than the duration of similar sounds in T. lastoviza.
Maximum amplitude of oscillations of all three types
of sounds is observed at a frequency of approximately
500 Hz. During feeding of E. gurnardus, sounds of the
type of knocks are heard most frequently (10 sounds
per minute); sounds of the type of grunts are heard
more seldom (4.5 sounds per minute). Sounds of the
type of growls (0.3 sounds per minute) are the rarest

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

992 KASUMYAN

Fig. 18. Acoustic signaling in Eutrigla gurnardus at concurrent feeding: fish from the left emits knocks during seizing a prey and
subsequent flight, and fish from the right emits whistle or grunts at frontal display. Oscillograms show sounds emitted by interact
ing individuals; the length of a horizontal fragment corresponds to 10 ms (Amorim, 1996; Ladich and Myrberg, 2006).

and are recorded mainly at the end of the grunts
sounds (Amorim and Hawkins, 2000; Amorim et al.,
2004b).
Beyond the feeding period when there is no food in
the basin, Triglidae of both species seldom emit sounds
and stay most of the time either immovable on the
ground or slowly move over it, using the free rays of the
pectoral fins. The situation changes drastically when a
small portion of feed is placed into the basin. If a frag
ment of the feed descends to the bottom near a single
standing fish, it quietly seizes it and moves with it to a
more isolated place. Quite a different picture is
Frequency, %
60
50
40
30
20
10
0 no relationship between the frequency of sound gener
1 2 3 4 5 6 7 8 9
Elements of feeding concurrent behavior
Fig. 19. Frequency of manifestation (in %) of elements of
concurrent feeding behavior (light columns) and sound
generation (dark columns) in Triglaporus lastoviza.
(1) Free swimming and an undirected food seach, (2) cir
cling near food and competitors, (3) seizing of food,
(4) retaining and swallowing of the serized food, (5) orien
tation in direction to a competitor, (6) approach to a com
petitor on the bottom or during swimming, (7) frontal
demonstration (spread of pectoral and dorsal fins and
positioning on the ground so that the head was directed at
the competitor’s head), (8) touching of the competitor by
free rays of pectoral fins, rostrum, or body, and (9) rapid
moving away from a competitor (according to data of
Amorim and Hawkins, 2000).
observed when feed is placed near two to three fish. In
such a situation, the feed that appeared initiates in fish
located not far from it concurrent behavior, in which
eight to nine different elements are distinguished. At
first, fish make a dart to the feed trying to be ahead of
competitors, however, seizing of the feed immediately
after it is descended to the bottom of the basin occurs
seldom. Fish can circle near feed making no attempts
to seize it, exhibit an undirected food search, orienta
tion for a competitor, approach a competitor over the
bottom or during swimming, spread pectoral and dor
sal fins, and position on the ground so that the head
was directed at the head of a competitor (frontal dem
onstration). Such behavior can be repeated several
times and usually for some time retains competitors
from attempts to grasp feed. In gray gurnard, frontal
demonstration precedes feed seizing in 40% of cases
(Fig. 18) (Amorim and Hawkins, 2000; Amorim et al.,
2004b).
Sound emission in Triglidae is considerably related
to precisely the manifestation of competitive behavior;
however, there is no direct relationship between the
frequency with which the interacting individuals
exhibit this behavior and sound generation. There is
ations and the number of competing individuals either.
In T. lastoviza, sound emission is most frequently
observed when fish seizes feed, even in those cases
when seizings from the ground surface occur in the
absence of actual feed (Fig. 19). Sounds frequently
arise during circling of fish near feed or near competi
tors, if a fish emits a sound at this time, it is more prob
able that it will be followed by a rapid feed seizing. Cir
cling of a silent fish usually does not lead to feed seiz
ing. In E. gurnardus that emits three different types of
the sounds, knocks are most typical of cases when a
fish seizes feed, when it rapidly approaches the feed,
but does not seize it, and when it circles near the feed.
Sounds of the type of grunts are observed most fre

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

 ACOUSTIC SIGNALING IN FISH
quently during agonistic manifestations, such as fron
tal demonstrations. It is assumed that the knocks
sound can reflect the feeding excitation of fish caused
by the appearance of the food, as well as serve as a
warning or repellent signal for competitors. Sound of
the type of grunts accompanying frontal demonstra
tions signals about aggressive intentions of an individ
ual emitting this sound (Amorim and Hawkins, 2000;
Amorim et al., 2004b). With age, the aggressiveness in
E. gurnardus decreases; therefore, larger individuals
less frequently produce grunts and more frequently
emit knocks (Amorim and Hawkins, 2005). Vocaliza
tion related to feeding is typical also of other species of
Triglidae—Prionotus carolinus and P. evolans (Fish,
1954).
Sounds associated mainly with feeding behavior
are rather comprehensively studied—in gudgeon
G. gobio, a freshwater gregarious cyprinid fish that, as
Triglidae, most part of the time is engaged in foraging
on the bottom or in the bottom ground. Sounds of
gudgeon resemble creak or croak and represent, in a
majority of cases (60%), a single series of 1–11 acous
tic pulses (on average 5 pulses); the duration of each of
them is 2 ms. The dominant frequency of sounds varies
from 1 to 2 kHz. In general, the duration of a single
series is approximately 20 ms. Two to five such series
follow each other less frequently (in 30% of cases) and
more than six series more frequently (10% of cases).
Gudgeon emits sounds in different situations, but only
when it is in a school. In a half of cases, sound gener
ation is a response of an individual that noticed near it
another partner of the school digging in the ground.
The appearance of such fish causes not only sending of
an acoustic signal, but also a behavioral response—the
orientation at a fish occupied in search for food,
approach to it or swimming round it, or initiates own
search for food in the ground (imitation). It is consid
ered that, using sounds in gregarious fish, such as gud
geon, a certain distance can be maintained between
individuals in a school, especially at the moment of
their feeding (Ladich, 1988). It is known that feeding
competition within a school of fish is clearly pro
nounced (Krause and Ruxton, 2002). In another gre
garious fish, Atlantic cod, under conditions of concur
rent feeding, no intensification of sound generation
occurs; however, fish sounding can increase some time
after feeding, as is assumed, in connection with an
increase in the general level of excitation and aggres
siveness of fish caused by the proper process of feeding
(Brawn, 1961b). Knock sounds during feeding excita
tion are emitted by hungry large river perch Perca flu
viatilis when it notices that another more successful
perch seizes food. When emitting a sound, the perch
raises its dorsal fin, and then can begin to pursue the
competitor (Protasov and Romanenko, 1962).
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11
993
SPECIFICITY OF FISH SOUNDS
Species Specificity of Sounds
Sounds emitted by fish of different species usually
clearly differ. Species specificity of sounds of fish
belonging to the same family or genus, occupying sim
ilar ecological niches, and having overlapping ranges
has been demonstrated up to now by many examples.
It was shown that closely related species have different
acoustic repertoires, in which uniform sounds differ in
acoustic parameters. For instance, among Scianidae,
there are species characterized by a wide diversity of
produced sounds (Cynoscion nebulosus) and species
that in different situations are capable of generating a
sound of only one type (Connaughton et al., 2000);
Gilmore, 2003; Ramcharitar et al., 2006). Sounds of
Gadidae are clearly distinguishable in duration and
frequency of sequence of pulses (Hawkins and Ras
mussen, 1978). The territorial males of two freshwater
North American Etheostoma nigripinne and E. cros
sopterum (Percidae) in the reproduction period pro
duce sounds of three types: “knock,” “purr,” and
“drum.” The “drum” sound has a harmonic structure,
“knock” and “purr” sounds (the latter is produced
only by males of E. nigripinne) belong to pulse sounds
of nonharmonic nature. Uniform sounds of males of
E. nigripinne and E. crossopterum differ in the number
of pulses and the frequency of sequence of pulses in
series, as well as in sound duration. Sounds of natural
hybrids between these species have with respect to
some parameters intermediate values as compared to
sounds of parental species (Table 3) (C. Johnston and
D. Johnston, 2000a).
Males of sympatric species of the genus Pomacen
trus (P. partitus, P. fuscus, P. leucostictus, P. plantifrons,
P. variabilis) inhabiting coral reefs emit during court
ship behavior and during protection of own sites
within small colonies short sounds resembling chirps.
The acoustic characteristics and structure of these
sounds in all studied species of Pomacentrus are close
(series of 3 pulses, duration of pulses and series, 7–15
and 40–60 ms, respectively; maximum amplitude in
the range of frequencies, 250 to 1000 Hz). Sounds
have an interspecies effect; however, the highest effi
ciency in stimulation in males of courtship behavior is
observed, nevertheless, in response to their own
sounds. This clearly indicates the capability of these
closely related sympatric fish to distinguish each other
according to acoustic signals (Myrberg and Spires,
1972). Sounds of Chromis chromis resemble signals
produced by a closely related species, C. viridis, but
have a more narrow frequency range and a smaller
dominant frequency (Amorim, 1996). Comparison of
sounds of aggression in 14 species of the genus
Amphiprion and other fish of the family Pomacentridae
indicates that their acoustic signals differ in dominant
frequency, number of clicks or creaks in series, and
number and duration of single acoustic pulses forming
clicks and creaks (Amorim, 1996).
2009
994
(a)
(b)
(c)
(d)
0 1 2 3 4 5
Time, s
Fig. 20. Oscillograms of sounds of three species of Carapidae in two different time scales (Parmentier et al., 2003): (a) Carapus
boraborensis, (b) C. homei, and (c, d) Encheiliophis gracilis.
Sounds of Carapidae—Carapus boraborensis,
C. homei, and Encheiliophis gracilis are easily distin
guishable in their structure. They differ in the number
of knocks (acoustic pulses) in a series and in duration
of intervals between knocks, as well as in frequency
(Fig. 20) (Parmentier et al., 2003). Similar conclu
sions follow from comparison of sounds of some other
closely related species, including sympatric species
(Gerald, 1971; Myrberg et al., 1978; Spanier, 1979;
Myrberg and Spines, 1980; Lobel, 1998), as well as of
fish not only of those found in common, but also of
those whose divergence into independent species is
possibly not terminated. This can be exemplified by
Cichlidae from Lake Malawi where, according to dif
ferent estimates, 450 to 650 species that formed as a
result of a progressing adaptive radiation dwell
(Turner, 1999). It was elucidated that males of differ
ent species of the genus Pseudotropheus from Lake
Malawi during courting a female generate lowfre
quency sounds that, despite a considerable interspe
cies similarity, nevertheless significantly differ in
parameters such as dominant frequency and number
and duration of pulses in a sound. Among the studied
species of this genus, the most pronounced differences
in acoustic parameters of sounds were found in
P. emmiltos and P. fazilberi that inhabit in common
KASUMYAN
6 0 200 400 600 800
Time, ms
one of the sites of the lake. It is noteworthy that pre
cisely fish of these two species are close in color and
specific features of drawing on the body. It is assumed
that acoustic signaling together with visual signaling
and, possibly, with olfactory one can provide recogni
tion of each other by these fish dwelling in common
(Amorim et al., 2004a, 2008).
Sounds differ in two wellstudied species of toad
fish, O. tau and O. beta, whose ranges overlap. The
inviting sounds of males of O. tau are relatively simple;
they consist of only one tonal element and last, on
average, for approximately 300 ms. The sounds of
males of O. beta are considerably more complex; they
include a preceding element (grunt), followed by sev
eral tonal elements, and the total duration of a sound
usually considerably exceeds 1000 ms. The dominant
frequency of the sound of these species also differs—
approximately 200 Hz in O. tau and almost 300 Hz in
O. beta (Fine, 1978; Thorson and Fine, 2002a).
Among Batrachoididae, the widest set of sounds emit
ted in the spawning period is typical of Lusitanian
toadfish Halobatrachus didactylus. Its acoustic reper
toire, besides sounds of the type of “boatwhistle” and
“grunt” includes diverse short sounds of the type of
croak and double croak and mixed sounds consisting
of squeaks and croaks ((Fig. 21) (Dos Santos et al.,
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
2000). A sound of the “boatwhistle” type begins and
terminates by grunts, has a prolonged tonal element,
with a duration, on average, of approximately 800 ms,
dominant frequency of approximately 60 Hz, and
numerous harmonics, among which the second or
fourth dominate. Grunts follow in series, on average,
of eight elements, each of which has a duration less
than 100 ms with a dominant frequency of approxi
mately 300 Hz. The dominant frequency of single and
double croaks is approximately 650 and 500 Hz,
respectively. Short sounds, croak, and double croak
are emitted also beyond the reproduction period and,
as is assumed, can be related to regulation of agonistic
relations in Lusitanian toadfish (Amorim, 2006;
Amorim et al., 2006). Sounds differ in two species of
Polypterus—P. senegalus and P. retropininnis, both in
their characteristics and diversity: P. retropinnis emits
sounds of two types—relatively prolonged moans,
with duration of approximately 290 ms and the domi
nant frequency of 50–150 Hz and short thumps with
duration of 67.4 ms and the dominant frequency of
100–200 Hz. P. senegalus produces only thumps that
are more prolonged (81.5 ms) than in P. retropinnis
(Ladich and Tadler, 1988).
Noteworthy in this respect is an example of species
of the genus Pollimyrus (Mormyridae) that frequently
occur in the same water bodies in West Africa. Males
of Pollimyrus, in the spawning period, emit inviting
sounds to attract females to their nest territories. Male
sounds are complex in structure and represent alterna
tion of three simple sounds—moans, grunts, and
growls. The order of sequence of simple sounds, their
number and duration, frequency and interpulse inter
vals are specific for each studied species of Pollim
myrus. In sounds of P. adspersus, moans and grunts
alternate, sometimes they are followed by prolonged
growls; in sounds of P. isidori, a single grunt is followed
by several moans. In sounds of P. marianne, either only
moans are present and there are no grunts (average
duration of 1.9 s) or moan and grunt are emitted
simultaneously, or a prolonged moan with several
grunts that coincide with it in time and follow each
other (average duration of 14.9 s). The latter indicates
the possibility of using by fish of two different mecha
nisms of sound generation simultaneously. The fre
quency of sequence of pulses in sounds of the same
type differs considerably (almost twofold). For
instance, in grunts of P. marianne, pulses follow with a
frequency of 34 Hz, in P. isidori they follow with a fre
quency of 44 Hz, and in grunts of P. adspersus they fol
low with a frequency of 56 Hz. Growls or buzz occur
ring in sounds of P. adspersus are lacking in P. isidori
and P. marianne. The acoustic characteristics of
moans and grunts of all three species of Pollimyrus also
differ (Fig. 8, Table 4). All this allows to correctly
identify species belonging of Pollimyrus from the oscil
logram of their sounds (Crawford, 1997a, 1997b;
Crawford and Huang, 1999). Differences in acoustic
characteristics of moans and grunts were revealed also
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11
995
(a)
500 ms
(b)
100 ms
(c)
100 ms
Fig. 21. Oscillograms of sounds of Lusitanian toadfish
Halobatrachus didactylus: (a) boatwhistle, (b) grunt, and
(c) double croak (Amorim et al., 2006).
during comparison of two sympatric species of Pol
limyrus, P. marianne, and P. castelnaui, whose ranges
do not overlap but are close to each other. It is of inter
est that the sounds (moans) of fish caught in the zone
of a limited contact of ranges of these two species in
duration and some other temporal parameters are sim
ilar to sounds of P. marianne, while in other parame
ters (frequency) resemble sounds of P. castelnaui
(Lamml and Kramer, 2006).
Comparison of sounds of Pollimyrus indicates that
species specificity of complex sounds in fish is reached
due to differences in temporal characteristics—fre
quency of sequence of pulses and the interval between
them in simple sounds, different sequence and dura
tion of simple sounds, as well as due to frequency
amplitude characteristics. Pollimyrus, as Mormyridae
in general, belong to so called auditory specialists
characterized by high hearing capabilities. The range
of frequencies in which the best hearing parameters
are observed in Pollimyrus coincide with the frequency
dominant in sounds they generate (Crawford, 1993).
Specific features of produced sounds, their correspon
dence to auditory capabilities of fish, and the mode of
life and spawning of these fish indicate undoubtedly an
important role of acoustic signaling not only in the
regulation of spawning behavior in Pollimyrus, but also
in provision of reproductive isolation of these fish that
2009
996 KASUMYAN
are often found in common in the same water bodies
and inhabit similar biotopes in them.
The capability of fish to differentiate sounds that
often differ slightly in their acoustic characteristics
agree with data on the functional abilities of the audi
tory system in fish, in particular, the ability to differen
tially respond to a sound with maximum short inter
pulse intervals (with duration up to 1.5 ms) (McKibben
and Bass, 2001; Wysocki and Ladich, 2003). In the
secondary auditory centers located in torus semicircu
laris, audirtory neurons exhibiting an extremely high
specificity to acoustic signals with strictly definite
interpulse intervals were found (Crawford, 1997b). It
is considered that precisely temporal characteristics of
sounds—the duration of interpulse intervals and
duration of proper pulses, as well as the number of
pulses in a sound and the duration of proper sound
serve as principal characters, according to which fish
can recognize near remote auditory signals (Spanier,
1979; Crawford et al., 1997a).
Undoubtedly, species specific features of sounds
facilitate the interaction between conspecifics, which,
in turn, decreases the probability of interspecies
hybridization between closely related species, espe
cially in those cases when they inhabit the same water
bodies, occupy in them similar biotopes, and are close
in demonstration of reproductive behavior. However,
it should be noted that differences between sounds of
closely related species can be poorly pronounced or
even absent if their ranges do not overlap. For
instance, sounds emitted during signal jumps by males
of two allopatric species of the genus Dascyllus:
D. albisella and D. trimaculatus do not differ either in
the number of pulses or in interpulse interval (Spanier,
1979; Mann and Lobel, 1998). During invasions when
zones of distribution of two previously isolated closely
related species overlap, crossing is observed between
them, as, for instance, in the case of an endemic of the
Hawaiian Islands–green damselfish A. abdominalis
and IndoPacific A. vaigiensis that penetrated here
(Maruska et al., 2007). The sounds of closely related
species can have also common features. For instance,
comparison of sounds of four North American species
of the genus Cyprinella revealed that sounds emitted by
males during aggression and courting a female are
most similar in C. gibbsi and C. trichroistia—sister spe
cies occurring in closely situated water bodies. Sounds
of males of C. galactura and C. callisema differ more
strongly, not only in acoustic characteristics, but also
in behavioral situations in which they are generated by
males (Phillips and Johnston, 2009). These results
indicate a definite relationship between the sound
similarity and the phylogenetic closeness of fish.
Population Differences in Sounds
There are few data on sounds emitted by individu
als that belong to different geographically distant or
isolated populations. Evidence obtained for huddock
JOURNAL OF ICHTHYOLOGY
from the northwestern Atlantic and the North Sea
allows to conclude that noticeable population differ
ences in fish in diversity of their acoustic repertoire
and the acoustic characteristics of sounds are evidently
either absent or these differences are insignificant
(Hawkins and Amorim, 2000; Bremner et al., 2002).
Similar results were obtained during comparison of
sounds emitted by males of Hawaiian dascyllus
D. albisella during signal jumps. No considerable dif
ferences were found between sounds recorded in colo
nies of these fish off the Hawaiian Islands and near
Johnston Atoll situated 1000 km away from them
(Mann and Lobel, 1998). Differences in the dominant
frequency found while comparing sounds of males of
oyster toadfish O. tau from northern and southern
populations (coast of the states Delaware, Virginia,
and South Carolina, United States) are insignificant
and can be caused by different temperature conditions
and different hormonal status of fish in the observation
period (Fine, 1978). However, in Amphiprion akallopisos,
the geographic variability of sound parameters was
found, which can indicate the specialization of sound
generation in fish to particular conditions of their
existence (Parmentier et al., 2005). Similar results
were obtained in comparison of sounds of aggression
and courting a female in males of Cyprinella galactura
(Phillips and Jonston, 2008b).
Individual Specific Features of Sounds
The available observations show that fish possess an
individual acoustic signature. For instance, in differ
ent males of two species of Pollimyrus, P. adspersus and
P. isidori, the frequency of sequence of pulses and the
dominant frequency in inviting sounds do not coin
cide, and these individual acoustic specific features are
stable in time (Crawford, 1997a). The performed elec
trophysiological studies show that even small differ
ences in sounds are perceived by the auditory system.
In P. adspersus, the frequency differential sensitivity in
the range of highest sensitivity to tonal sounds (100–
500 Hz) is approximately 9 Hz. The capability to dif
ferentiate the slightest changes in the interpulse inter
val is also well developed. In sounds with an interpulse
interval of approximately 10 ms, fish recognize its
increase or decrease as slight as by 0.3 ms, at interpulse
intervals of approximately 40 ms, changes by 3 ms are
significant (Marvit and Crawford, 2000), Considering
high auditory capabilities of Pollimyrus, it is suggested
that females can differentiate and assess males from
their individual acoustic signature and use this capac
ity for orientation and during choice of a spawning
partner (Crawford, 1997a). According to field obser
vations, male density distribution at spawning sites is
rather high, and a female can hear simultaneously sig
nals of four to five males (Crawford, 1997b). Under
artificial conditions at keeping mature P. adspersus in
common, a multiple spawning of a female with the
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
same selected by it partner was recorded (Crawford,
1997a).
The possibility for recognition of individuals
according to sounds was revealed in other fish also. In
colonies of bicolor damselfish, the territory that
became free after removal of the male host is occupied
by neighbors of the colony much more rapidly if
recordings of sounds belonging to other males rather
than to the former host of the territory are retransmit
ted (Myrberg and Riggio, 1985; Myrberg, 1997). Indi
vidual differences in sound duration were found in
Argyrosomus regius, frequency of generation of acous
tic series is maintained constant by each individual
during tens of minutes (Lagardère and Mariani, 2006).
The individual variability of sound generation is
clearly seen against the background of a high stability
of acoustic characteristics of sounds of an individual.
For instance, in males of Zosterisessor ophiocephalus,
the frequency of sequence of pulses in sounds varies
from 21.8 to 68.3 per second; they follow with strict
regularity in sounds of each male (Malavasi et al.,
2003). In the inviting sounds of oyster toadfish O. beta,
the sound frequency and amplitude are least variable,
and the sound duration is less stable (Bazimo and
Fine, 1998). Males of Lusitanian toadfish H. didacty
lus are clearly distinguishable according to sound
duration and some frequency characteristics. The
variability of sounds produced by different males was
always higher than differences between sounds emitted
by the same males (Amorim and Vasconselos, 2008).
The individual acoustic signature is evidently retained
by fish throughout their life. At least, males of O. beta
with the same sound parameters were found at the
spawning grounds not only in different periods of the
spawning season, but also in different years (Thorson
and Fine, 2002a).
SPAWNING THAT ACCOMPANIES SOUND
GENERATION
At the moment of sound generation, many fish per
form certain movements or assume typical postures
that in several cases are related to the work of the cor
responding soundgenerating mechanism. Lined sea
horse Hippocampus erectus, when emitting a clicking
sound, raises its head. Such movement is necessary for
adjoning bones of the occipital part of the cranium to
displace with respect to each other and cause the
appearance of a stridulation sound (Colson et al.,
1998). In Polypterus retropinnis and P. senegalus at the
moment of sound emission, one can observe a spread
of dorsal fins and vibration of body walls that cover a
long swimming bladder used by these fish for aerial
breathing—abdominal wall between pectoral and ven
tral fins and the lateral wall from ventral fins to a cau
dal fin. Wall vibration occurs in time with thump
sounds that can be generated singly or in series with
maximum rate to three sounds per second during a
minute and more (Ladich and Tadler, 1988). When
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
997
emitting sounds, European perch P. fluviatilis raises its
dorsal fin (Protasov and Romanenko, 1962). In silver
sweeper P. schwenkii, at the moment of generation,
fins are not spread, but vibration of walls of the
abdominal cavity in the region of the swimming blad
der becomes clearly noticeable (Takayama et al.,
2003). During sound generation in cuskeel O. mar
ginatum, slight head vibration is noticeable (Mann
et al., 1997). Such movements serve as an external
manifestation of the work of tympanic muscles in
these fish. In Cichlidae, in which tympanic muscles
were not found, vocalization usually (not always) is
accompanied by quivering of the abdominal wall
(Lobel, 1998, 2001; Amorim et al., 2003). Males of
Padagobius nigricans during sound generation lower
their gill membrane, move aside operculi, and quiver
with pectoral fins (Lugli et al., 1996). Gudgeon
G. gobio during sound emission raises its dorsal fin and
turns its head and the anterior part of the body to the
right and to the left. Such turns follow in time with a
series of acoustic pulses, at the moment of turn, the
swimming fish changes the direction of movement,
and a fish resting on the bottom, displaces (Ladich,
1988). Gudgeon G. gobio at the moment of generation
of an agonistic sound—a single knock—produces a
typical nod with its head and, owing to special and well
developed musculature, rapidly draws to itself gill
membrane and operculi, and, together with them,
large ventral fins. Such movements follow each other if
a fish emits a series of knocks (Ladich, 1989). Botia
modesta, during emission of warning clicks, slightly
moves forward and rapidly opens and shuts its mouth
(Raffinger and Ladich, 2009).
Visually, the moment of sound generation in fish
can be not pronounced; however, fish at this time can
assume certain postures. John dory Z. faber at the
moment of sound emission spreads dorsal and anal
fins; it occurs not only in water, but also when fish is
removed from water and held in hands. Sound genera
tion in John dory is not a consequence of fins move
ments, but is related to the work of the tympanic
soundgenerating apparatus (Onuki and Somiya,
2004). Males of oyster toadfish O. tau for production
of inviting sounds slightly move forward in the direc
tion of the exit from the nest shelter. The posture and
location of a male in a shelter are rather typical: a male
remains in the nest, but positions in it so that its head
up to the line of the eyes protrudes beyond the shelter
boundaries. At the moment of sound generation, the
male is immobile (Barimo and Fine, 1998). Males of
Etheostoma nigripinne and E. crossopterum (Percidae)
also retain immobility during sound production
(C. Johnston and D. Johnston, 2000a).
RHYTHMS OF ACOUSTIC ACTIVITY OF FISH
The fact that the acoustic activity of fish does not
remain constant but emerges, disappears, or changes
throughout 24 h or during an annual cycle was noticed
998
Frequency of sounds during 10 min
35
30
25
20
15
10
5
11
Fig. 22. Diurnal dynamics of emission of sounds of the type of moan and grunt in males of Pollimyrus marianne (Lamml and
Kramer, 2005).
as early as at the beginning of study of fish bioacous
tics. With the development of these studies and data
accumulation, the existence of clearly pronounced
diurnal and seasonal rhythmicity of sound generation
in fish became more obvious.
Diurnal Rhythmicity
In many studied fish, maximum of acoustic activity
is observed at twilight or dark time of the day, and con
siderably less frequently sound generation occurs in
the day hours. Such diurnal rhythm is typical of repre
sentatives of the numerous family Sciaenidae. For
instance, Roncador stearnsi, Umbrina roncador, and
Sciaena saturna dwelling off the coasts of California
begin their “chorus singing” regularly each day after
sunset. These fish emit sounds during a limited time
interval—only for approximately 2.5 h (Fish, 1969).
In gray weakfish C. regalis, during the reproduction
period, acoustic activity is maintained at a high level
throughout most part of the day, but decreases to min
imum in the middle of the day. With the onset of
evening twilight, the generation of drumming sounds
by males rapidly reaches maximum and remains such
up to late night. The maximum of generation of drum
ming sounds is slightly ahead of time of proper spawn
ing of gray weakfish, which indicates that sounds likely
promote the formation of spawning aggregations.
According to slight shifts in time of the onset of maxi
mum acoustic activity of fish in the offshore and at a
distance from it, it is possible to trace movements of
spawning aggregations during 24 h (Connaughton and
Taylor, 1995). Acoustic activity changes in the same
manner also in other representatives of the numerous
family Scianidae—Cynoscion xanthulus, C. nebulosus,
Pogonias cronis, Nibea albiflora, Argyrosomus argenta
tus, etc. (Shishkova, 1963; Protasov, 1965; Fish and
KASUMYAN
Day Night Day
“Moan”
“Growls”
13 15 17 19 21 23 1 3 5 7 9 11
Hours
Cummings, 1972; Takemura et al., 1978; Saucier and
Baltz, 1993).
Males of cuskeel O. marginatum that spend day
hours in the ground begin to vocalize before sunset,
prior to coming out of the ground. A slow leaving of
the ground in these fish occupies approximately
20 min. During this time and in the subsequent min
utes, vocalization increases, reaches maximum an
hour after sunset, and then rapidly decreases (Mann
et al., 1997; Rountree and BowersAltman, 2002).
Regularly every day after sunset, Anisotremus davidsoni
(Haemulidae) begins its “chorus singing” (Fish,
1969). A distinct attribution of vocalization to a dark
time of the day is exhibited by Pollimyrus marianne.
Emission of any sounds in these fish begins immedi
ately after sunset and ceases completely with the sun
rise (Fig. 22) (Lamml and Kramer, 2005). The fre
quency of sound generation drastically increases with
the onset of evening twilight in Opsanus. If before sun
set, males of these fish emit inviting sounds seldom, on
average, one sound per each 7.5 min, immediately
after sunset, sounds are heard every 2 min, and upon
half an hour, there are already two sounds per minute.
Together with an increase of the emission frequency of
sounds, their duration and the number of repeated
tonal elements (simple sound loops) forming complex
sounds of males of Opsanus decrease (Fig. 23)
(Thorson and Fine, 2002a).
An increase of vocalization in the evening or morn
ing hours of twilight illumination is typical of marine
and freshwater fish of different taxonomy—for Sebas
ticus marmoratus (Scorpaenidae) (Miyagawa and
Takemura, 1986), Galeichthys felis (Ariidae) (Breder,
1968), Holocentrus rufus (Holocentridae) (Winn,
1964), Botia berdmorei (Cobitidae) (Rigley and Mar
shall, 1971), and Puntazzo puntazzo (Sparidae) (Shish
kova, 1963; Protasov, 1965). The same diurnal rhyth
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH 999

(a) 1 Number of sounds during one hour

150
2
Number of sounds
4

Sound duration, ms
1500

100
1000 3

50 500 2

1 2 3 4 5 1
30min intervals
(b)
elements in a sound

0 4 8 12 16 20 24
Number of tonal

3
h
2
Fig. 24. Diurnal dynamics of acoustic activity in males of
1 Abudefduf luridus protecting their territories from other
fish (total for four males). Arrows show the time of sunrise
and sunset (Santiago and Castro, 1997).
1 2 3 4 5
30min intervals

Number of swimming fish, M ± m

5
Fig. 23. Inviting sounds of males of oyster toadfish Opsanus
beta during 30min intervals prior and after the onset of
evening twilight: (a) (1) frequency of emission and 4
(2) duration of sounds and (b) number of tonal elements in
sounds. The arrow shows the time of sunset (Thorson and 3
Fine, 2002a).

micity of sound generation is exhibited also by highly
aggressive males of damselfish A. luridus and other
Pomacentridae fish, in whose behavior visual recep
tion is dominant (Fig. 24) (Myrberg, 1972; Mann and
Lobel, 1995; Santiago and Castro, 1997).
There are less examples when maximum of acous
tic activity in fish is in the light hours of the day. Such
rhythm of vocalization was recorded in Notropis
analostanus (Winn, 1964), as well as in Atlantic cod, in
which acoustic activity is considerably higher in the
day hours than at night (Midling et al., 2002; Finstad
and Nordeide, 2004). During the light hours of the day
and in the morning and evening twilight, males of had
dock mainly vocalize; these fish seldom emit sounds at
night, although the repertoire in general retains its
diversity (Hawkins and Amorim, 2000). A strict
occurrence of sound production in the day hours is
observed in Labrus viridis, Crenilabrus greseus, and
Trachurus trachurus (Protasov, 1965), and in Eutrigla
gurnardus that is a typical daytime fish (Fig. 25)
(Amorim, 2005). At the dark time of the day, in these
fish, not only sound production attenuates, but also
locomotor activity and manifestation of different
social (intragroup) and other contacts decrease. How
ever, in other closelyrelated species from the family
Triglidae, maximum acoustic activity is recorded after
sunset at twilight illumination (Protasov and Aronov,
1960; Protasov and Romanenko, 1962). Thus, the
diurnal rhythm of sound generation differs even in
closely related fish and is intimately associated with
2
1
2 4 6 8 10 12 14 16 18 20 22
h
Fig. 25. Diurnal dynamics of locomotor activity of Eutrigla
gurnardus. The vertical is the average number of moving
individuals of five fish simultaneously present in the basin.
Dark, gray, and light fragments at the horizontal diagram
reflect the dark, twilight, and light time of the day
(Amorim, 2005).
their diurnal rhythmicity of behavior. The absence of
pronounced diurnal fluctuations in sound production
was recorded only in a small number of species
(Ladich, 1988, 1989).
Seasonal Rhythmicity
Seasonal cyclicity of acoustic activity in most
vocalizing fish is distinctly pronounced. Throughout a
year, maximum vocalization occurs usually in the
reproduction period when, in many fish, profound
changes in physiology and behavior take place. Some
fish produce sounds only at this time and are silent for
the remaining part of the year. Their acoustic activity
rather strictly coincides with the dates of spawning and

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

1000
Sound activity, arb. units 4 2
3
2
0 20
Apr. 20 May 20 June 19
Dates
Fig. 26. Acoustic activity of males of gray weakfish Cynos
cion regalis in the offshore of Delaware Bay in the spawning
period: (1) drumming sounds and (2) chirps. Conventional
units: (0) absence of sounds, (1) less than 30 sounds per
minute, (2) 30–50 sounds per minute, (3) continuous
emission of several individuals, and (4) continuous emis
sion of several fish (Connaughton and Taylor, 1995).
can serve as a peculiar indicator of the beginning of the
reproduction season. For instance, cuskeel O. mar
ginatum (Ophidiidae) emits sounds only in the repro
duction period, which is used not only for the determi
nation of the dates and duration of spawning, but also
of sites of distribution of these secretive and difficult to
discover fish (Rountree and BowersAltman, 2002;
Rountree et al., 2006). A strict seasonality in sound
generation is demonstrated by many Sciaenidae fish,
for instance, well studied gray weakfish C. regalis
dwelling off the Atlantic coast of North America. At
sites of spawning, gray weakfish begins to emit typical
drumming sounds in spring, their intensity rapidly
reaches maximum by midMay, and towards the end
of July almost completely ceases (Fig. 26). The
dynamics of acoustic activity well coincides with the
gonad condition in fish in catches and with the sizes of
tympanic muscles, which in males by this time
increase almost threefold (Connaughton and Taylor,
1994, 1995). Maximum generation of another sound
that is attributed to gray weakfish, chirps or chattering
is shifted to later dates and occurs by the moment of
spawning termination. The precise purpose of this
sound arising during rubbing of pharyngeal teeth
remains unclear (Connaughton and Taylor, 1995). It is
likely that chattering is related to the beginning of the
postspawning feeding of fish. It should not be excluded
either that the chattering sound is produced by some
other fish rather than by gray weakfish (Sprague and
Luczkovich, 2001).
Interesting data on the seasonal variation of sound
production were obtained for Lusitanian toadfish
H. didactylus whose acoustic repertoire is distin
guished by a wide range and includes sounds of four
types: boatwhistle, grunt, single croak, and double
croak (Fig. 21). The performed yearround observa
KASUMYAN
1 3
2 (a) 1
2
Number of sounds per minute
3
1
(b)
July 19 Aug. 18
10
December
March
November
September
September
October
February
January
June
May
July
July
April
August
August
Fig. 27. Seasonal dynamics of sound generation in Lusita
nian toadfish Halobatrachus didactylus: (a) (1) growls,
(2) croaks, and (3) double croaks, (b) boatwhistle
(Amorim et al., 2006).
tions demonstrated that a sound of the boatwhistle
type is emitted by Lusitanian toadfish exclusively in
the reproduction period, from May to midJune. The
other three types of sounds are produced by fish during
the entire year; however, the frequency of generation
of grunts and double croaks in the reproduction season
drastically increases, and this peak coincides with the
time of emitting sounds of the boatwhistle type. The
production by Lusitanian toadfish of single croaks
does not undergo any pronounced seasonal fluctua
tions and is maintained at an equally low level
throughout the year (Fig. 27) (Amorim et al., 2006).
Inviting sounds of the boatwhistle type are produced
by males of O. tau also in spring immediately after
coming to shallow waters and distribution over shel
ters. An intensive vocalization of males calling up
females is limited to only five to six weeks; these typical
sounds are heard very seldom beyond the spawning
season. Females of O. tau possessing tympanic mus
cles, similar to males, do not produce such sounds,
although there is a potential capability for their gener
ation since such sounds are caused in females experi
mentally at an electric stimulation of neurons of the
motor acoustic nucleus (Winn, 1964, 1972; Fine,
1978). Only in the spawning period, sounds are emit
ted by plainfin midshipman (Acipenseridae), North
American Cyprinidae, and many others. The begin
ning and intensity of vocalization in fish in the spawn
ing season are related to serious displacements in the
state of sonic muscles induced by a hormonal splash,
which directly affects the ability of fish to maintain a
high acoustic activity in the reproduction period. The
acoustic parameters of sounds generated by fish,
except the level of sound pressure, remain as before,
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

78
Level of sound
76
pressure, dB
74
72
70
68
Frequency of sequence of
pulses in a sound, Hz
25
20
15
Fig. 28. Water temperature effect on the (a) level of sound pressure, (b) duration of acoustic pulses, (c) frequency of sequence of
pulses, and (d) the dominant frequency of the anxiety sound in gray weakfish Cynoscion regalis. The level of sound pressure is
expressed in dB relative to 1 µPa (Connaughton et al., 2000).
which indicates the localization of rearrangements
taking place at the level of periphery of the sonic
mechanism, rather than of the centers than control it
(Fine, 1978).
The intensity of sound production within a season
can vary, for instance, in relation to cyclic changes in
the physiological state of fish with multiple spawning.
In Hawaiian dascyllus D. albisella, whose reproduc
tion period continues during several months, maxi
mum vocalization in males occurs a day before spawn
ing and on the day of eggs deposition. Then during the
subsequent several days when a male is occupied with
displaying care of the batch, the intensity of sound
generation decreases; however, it again begins to dras
tically increase immediately after hatching of juveniles
when a male is ready again for reproduction (Mann
and Lobel, 1995). Similar intraseasonal fluctuations in
acoustic activity were found in other fish also (Craw
ford et al., 1986; Crawford, 1997a). In O. beta, the
generation of agonistic sounds (grunts) is related to
moon cyclicity: the acoustic activity of these fish
increases every 14–15 days with the onset of a new
moon and a full moon (Maruska and Mensenger,
2009). Moon cyclicity in sound generation is traced in
other fish also (Breder, 1968).
THE EFFECTS OF ENVIRONMENTAL
FACTORS
As most other processes and functions of fish,
sound generation depends on a powerful abiotic factor
such as water temperature. With an increase in water
temperature, the rate of exchange of calcium ions in
tympanic muscles responsible for sound generation
increases (Feber et al., 1998), and, as a consequence,
the schedule of their work changes substantially,
JOURNAL OF ICHTHYOLOGY
ACOUSTIC SIGNALING IN FISH 1001
4.0
(b)
(a)
Duration of
3.8
pulses, ms
3.6
3.4
frrequency, Hz
(c) 600 (d)
Dominant
550
500
450
12 14 16 18 20 22 24 12 14 16 18 20 22 24
Water temperature, °C
which, in turn, is reflected in most parameters of
sounds produced by fish. In Polimyrus marianne and
7
P. adspersus, Q10 coefficient is close to 2.0 for the
amplitude of the sound of the moan type and for the
duration and frequency of sequence of pulses in grunt
sounds (Crawford et al., 1997a, 1997b; Lamml and
Kramer, 2005). In gray weakfish, in the temperature
interval of 12–23°C, the frequency of sequence of
pulses in an anxiety sound arising when fish are
removed from water for a short time also increases
almost twofold—from 13.4 to 24.3 pulses per second.
A distinctly pronounced positive linear dependence on
temperature is also exhibited by the level of acoustic
pressure of anxiety sounds and their dominant fre
quency while the duration of pulses with an increase in
temperature successively decreases (Fig. 28) (Con
naughton et al., 2000). The dominant (basic) fre
quency of sounds of males of plainfin midshipman
P. notatus, oyster toadfish O. tau, and Lusitanian
toadfish H. didactylus depends on water temperature
similarly (Fig. 29) (Fine, 1978; Brantley and Bass,
1994; Amorim et al., 2006). In Prionotus carolinus,
basic frequency increases by 43 Hz with an increase in
temperature by 2.5°C (Fig. 30) (Connaughton, 2004).
In Eutrigla gurnardus, the duration of pulses in sounds
of the grunt type noticeably decreases with a seasonal
increase in water temperature (Amorim, 2005).
A decrease in the duration of acoustic pulses, an
increase in the rate of their generation, and an increase
in the frequency of the sound and the level of acoustic
pressure that accompany water temperature increase
were found in many fish (Schneider, 1967; Fine, 1978;
7Q
10 coefficient means a change of the physiological or other
parameter at a change in water temperature by 10°C
Vol. 49 No. 11 2009
1002
Basic frequency, Hz
150
130
110
90
70
14 16 18 20 22 24 26
Water temperature, °C
Fig. 29. Dependence of the basic frequency of the inviting
sounds of males of plainfin midshipman Porichthys notatus
on water temperature (Brantley and Bass, 1994).
Basic frequency, Hz
230
220
210
200
190
15 16 17
Water temperature, °C
Fig. 30. Dependence of the basic frequency of anxiety
sounds on water temperature in northern searobin Priono
tus carolinus (according to Connaughton, 2004).
Bass and Baker, 1991; Connaughton et al., 2000). The
nature of these changes is related to temperature
effects on the work of the center regulating acoustic
activity and is common for all fish (Domski et al.,
1973; Bass and Baker, 1991). The intensification of
sound generation with water temperature increase
takes place parallel to an increase in the behavioral
activity of fish (Ladich, 1988).
An important factor affecting the acoustic activity
of fish can be a predator’s presence nearby. As was elu
cidated comparatively recently, sounds emitted during
hunt by bottlenose dolphin Tursiops truncatus drasti
cally suppress vocalization in O. beta. The inviting
sounds produced by males of O. beta unmask fish and
attract a predator (Gannon et al., 2005). Fish capable
of sound production in the feeding of bottlenose dol
phin comprise up to 80%; of them O. beta make up
more than 10% (RemageHealey et al., 2006). During
a hunt, bottlenose dolphin generates not only ultrasound
clicks that are inaccessible for reception O. beta, but also
lowfrequency pops in the range of 400–4500 Hz corre
KASUMYAN
sponding to its auditory perception (Nowacek, 2005).
The sounds of the feeding bottlenose dolphin exert the
same effect on the vocalization of some other fish also
(Luczkovich et al., 2000).
The noise background that is always present in an
aquatic medium well conducting acoustic oscillations
is also one of environmental factors affecting the abil
ity of fish to perceive valuable acoustic signals and
maintain acoustic communication. The strongest low
frequency noise background occurs in turbulence
zones, for instance, in the sea offshore or in rivers,
especially near rapids and bars. Some fish, in particu
lar, Cyprinidae, are rather sensitive to this factor and
can fully exhibit their high auditory abilities only at a
low environmental noise, for instance, in water bodies
with stagnant water. Against the noise background
present in running waters, the ability of Cyprinidae to
identify a valuable signal reduces drastically (Amoser
and Ladich, 2005). It was shown that fish, including
Cyprinidae such as roach Rutilus rutilus and rudd
Scardinius erythrophthalmus try to leave sites in the
water body where an increased level of acoustic pollu
tion is observed (Boussard, 1981, cited from Scholz
and Ladich, 2006). Mottled sculpin C. bairdi, as well
as, most likely, many other representatives of the fam
ily Cottidae, for acoustic signaling use sounds that dis
tribute in the bottom substrate rather than in water.
Such mode of signaling has certain advantages not
only because of a slower damping of acoustic oscilla
tions in the ground, but also thanks to an insignificant
penetration of various external noises to the bottom
18
substrate. This advantage is especially important for
fish living in a current, especially in zones of high tur
bulence, for instance, near river rapids, and bars
(Whang and Janssen, 1994). Fish inhabiting biotopes
where a large noise background is formed because of
high current turbulence can also use another strategy
to increase the efficiency of communication using
sounds. As was found, in smallsized Padogobius mar
tensii and P. nigricans inhabiting small rapid rock rivers
of Italy, the frequency range of the highest auditory
sensitivity and maximum amplitudes of emitted
sounds corresponds to the region where the level of
acoustic noises in the river is the lowest. Noise mea
surements in different sites of habitation of these fish
(near small waterfalls, at rapids, and in more quiet
places of the river) demonstrated that the so called
“acoustic window”—the range of frequencies in
which the noise level is low is located near 100 Hz, i.e.,
between lowfrequency noises related to water turbu
lence and the zone of higherfrequency noises caused
by bursts of air bubbles. The level of acoustic pressure
of acoustic noise in the river, even near rapids and
waterfalls, is, on average, 30 dB lower than the level of
the threshold of acoustic sensitivity of fish (Fig. 31)
(Lugli et al., 2003), which protects the auditory system
from functional overloads and damage of receptor
cells (Enger, 1981; Hastings et al., 1996; Scholik and
Yan, 2001). The fact that conditions even in the noisi
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
est sites of the river are quite suitable for spawning of
gobies is evidenced by a great number of their nests
near waterfalls and at a distance from them (Lugli
et al., 1992). The proximity of spectral zones of max
ima of auditory sensitivity and the amplitude of emit
ted sounds to the zone of external noises minimal in
intensity considerably increases the valuable sig
nal/noise ratio. The strategy directed at an increase of
the valuable signal/noise ratio by the generation of sig
nals getting into an “acoustic window” is typical also
for the acoustic communication of land animals, for
instance, birds and mammals (P. Waser and M. Waser,
1977; Ryan and Brenowitz, 1985).
Noises can be also of an artificial origin. The
sources of the anthropogenic pollution of water bodies
are mainly navigation, as well as seismic prospecting,
use of different underwater sonars, underwater works,
in particular, drilling of wells for oil and gas recovery,
and, finally, military operations. The issue how noises
can affect the life of fish and other underwater inhab
itants remains unclear in most cases, and distinct ideas
of the consequences of noise pollution for fish are
lacking. It is known that precisely at high levels and
long duration of noises, fish can lose hearing for a
short time, hence, capacities for acoustic communica
tion (Amoser and Ladich, 2003; Smith et al., 2004;
Kasumyan, 2005). Lowerintensity noise impacts can
induce different behavioral responses in fish. North
ern bluefinned tuna Thunnus thynnus in response to
the sound of a moving vessel changes its direction,
horizon and rate of swimming, the school becomes
more loose; the coordination of movements in fish
decreases, and rare agonistic manifestations between
the individuals of a school (demonstration of an
attack) can be observed (Sarà et al., 2007). Fish feel
the noise of highspeed motor boats at a distance of
300 m; such noises are for them potential stressors
causing an increase in cortisol level (Amoser et al.,
2004; Wysocki et al., 2006). The most dangerous
increased noise background that arises during move
ment of vessels can be for fish producing their own
sounds. As studies show, the frequency range of such
noises coincides with the zone of maximum auditory
sensitivity in fish, which leads to a considerable
increase in the threshold of sound perception, espe
cially in a lowfrequency region and, as a result, a
decrease in the distance at which the acoustic commu
nication of fish is possible (Vasconcelos et al., 2007).
An increase in grunts as a response stress reaction to
distant underwater explosions is observed in oyster
toadfish O. tau (Gray and Winn, 1961).
FORMATION OF ACOUSTIC SIGNALING
IN FISH ONTOGENESIS
The age when juveniles begin to actually use acous
tic signals for regulation of behavioral relations can so
far only be suggested. It is known that immature indi
viduals of some fish are capable of sound generation.
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11
1003
Sound pressure level, dB
130 1
120
110
100
90
2
80
3
70
70 100 150 200 300 400 500
Frequency, Hz
Fig. 31. (1) Audiogram of goby Padogobius martensii and
(2) spectrum of acoustic noise near small waterfalls and
rapids, and (3) in more quiet places of the small Stirone
River (average depth of 0.5 m, rocky bottom, northeast of
Italy) (Lugli et al., 2003).
For instance, large juveniles of Botia horae produce
clicks during protection of their territory (Valinski and
Rigley, 1981). Clicks are produced by juveniles of
Gnahtonemus petersi (Schneider, 1964a; Rigley and
Marshall, 1971), and juveniles of Terapon jarbua pro
duce drumming sounds. Juveniles of Hawaiian dascyl
lus D. albisella are capable of sound generation (Lobel
and Mann, 1995). How frequency and other parame
ters of sounds of fish juveniles correspond to their
auditory capabilities has been unclear for a long time.
Such estimates were made only in recent years with
reference to two species of Trichopsis—croaking
gourami T. vittata belonging to auditory specialists and
Lusitanian toadfish H. didactylus having no accessory
auditory structures.
Data obtained for the croaking gourami suggest
that acoustic communication in agonistic behavior
arises in juveniles much later than auditory sensitivity
and capacity to produce sounds (Wysocki and Ladich,
2001). In early juveniles, sounds have a low amplitude
and cannot be perceived by a still weakly developed
auditory system. During the first ten days of life, juve
niles do not exhibit any social relations. Beginning
from the 11th day, interrelations of the kind of
approach and flight are observed, by the 18th day, the
first lateral demonstrations with occupation of the so
called Tposture are recorded, and, by the 27th day,
pursuit is observed. Towards the age of 52 days, rapid
beatings with pectoral fins—movements that in adult
fish are associated with sound production—were
recorded. The first sounds were recorded on the 57th
day when they arise during lateral demonstrations of
2009
1004 KASUMYAN

Table 7. The time of manifestation of the first elements of agonistic behavior in ontogenesis of croaking gourami Trichopsis vit
tatus (according to Henglmüller and Ladich, 1999)
Age of juveniles,
Behavior
days after hatching
Approach (fish swims with spread out and slightly raised unpaired fins in direction of another individual) 11
Flight (moving to a side opposite an enemy) 11
Lateral demonstrations (fish, having widely spread out unpaired fins, stays near an enemy or with its head 18
perpendicular to its body⎯the so called Tposture or fish are located parallel to each other in the same
or opposite directions
Pursuits (following a moving away enemy) 27
Beatings with pectoral fins (rapid beatings with pectoral fins, often during lateral demonstrations 52
Sound emission 57
Frontal demonstrations and bitings of an enemy (enemies are located opposite each other, having 72
opened their mouths and usually tilting to a side and slightly bending their body, one of the fish
sporadically performs an abrupt jump and tries to bite the lips of the enemy)
Retreat (fish leaves the enemy, slightly tilting downwards and having pressed all fins to the body) 72

two conflicting individuals and beatings with pectoral
fins; other elements of agonistic behavior (frontal
demonstrations, bitings of lips of an enemy) arise later
(Table 7). During the subsequent 30 days, sounds are
recorded only in one of similar situations; however,
beginning from a threemonth age, each such contact
of fish is accompanied by sound emission. The fre
quency of manifestation of agonistic behavior and its
total duration rapidly increases in gourami with age,
the gap between the functional parameters of the
soundgenerating apparatus and auditory reception
disappears, and a possibility for acoustic communica
tion gradually is formed (Henglmüller and Ladich,
1999).
Results close in the meaning were obtained during
study of formation of auditory sensitivity and acoustic
characteristics of sounds in Lusitanian toadfish. Com
parative analysis shows that the auditory sensitivity of
juveniles with a length of less than 10 cm does not
allow them to perceive their own sounds that are insuf
ficiently high in amplitude. Such amplitude appears in
larger juveniles (12.4–15.3 cm) and in fish maturing
first (20.2–31.8 cm) whose sounds become still louder
and already exceed the threshold level of hearing
(Fig. 32). With an increase in age, the frequency of
sound in fish regularly decreases, but its amplitude and
duration of acoustic pulses increase; however, the
number of pulses in a sound decreases (Fig. 33). The
territorial juveniles of Lusitanian toadfish begin to
exhibit an agonistic behavior (mouth opening, spread
of pectoral fins at encounters of individuals with close
sizes) on reaching a body length of approximately
8 cm, which corresponds to an age of 1–2 years. How
ever, it is unlikely that the acoustic communication in
this age, despite the capacity of juveniles for producing
and perceiving sounds is actually exercised (Vasconce
los and Ladich, 2008). The orientation and attraction
to the sound source allows pelagic larvae of coral reefs,
as is assumed, to migrate from the open ocean to the
reef and find there suitable sites for settling where they
will stay for the remaining part of their life (Tolimieri
et al., 2000a, 2000b, 2004; Higgs, 2005; Simpson
et al., 2005). It is not ultimately established whether
this capacity is achieved owing to reception by larvae
of precisely acoustic signals or this behavior is regu
lated also by stimuli of another nature, for instance,
olfactory ones (Wright et al., 2005; Mann et al., 2007).
In Atlantic cod, the capacity for sound production
appears late, by the age of sexual maturation, on
reaching a body length of 25–37 cm (Brawn, 1961b).
In Tramitichromis intermedius, sound generation
begins only in mature individuals. Tracing of acoustic
activity with a periodicity of 4–5 days approximately
from onemonth age, when juveniles begin to swim
independently, showed that males begin to generate
sounds approximately 2–3 days before the first spawn
ing at the age of 7 months, and with each next day,
their acoustic activity increases almost twofold
(Fig. 34). The first sounds arise at the same time as the
first manifestations by maturing males of a specific
behavior observed in many Cychlidae fish at the
moment of generation—assuming by a male of a def
inite posture, spread of unpaired fins, interrupted
rapid flaps with pectoral fins, intensive undulating
movements with caudal peduncle, and flaps with the
caudal fin. Females in these fish produce no sounds.
Comparison of sounds emitted by wild individuals
caught in nature and by artificially reared fish showed
no significant differences (Ripley and Lobel, 2004).
This allows to make an important conclusion that the
capacity of fish to produce sounds with definite (spe
cific) characteristics for a particular fish species has an
innate nature.
The species acoustical pattern has also an innate
nature and is formed irrespectively of conditions the
fish are kept in during the embryonic and subsequent

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

 ACOUSTIC SIGNALING IN FISH 1005

(a)
120 1
2
100

80

60
Level of sound pressure, dB

120 (b) (d)

100

80

60

120 (e)
(c)
100

80

60
50

100

1000

1000
200
300

500

800

50

100

200
300

500

800
Frequency, Hz
Fig. 32. The (1) ratio of audiogram and the (2) spectrum of grunt sounds in different size groups of Lusitanian toadfish Halobatra
chus didactylus: (a) 2.8–3.8 cm, (b) 5.4–6.6 cm, (c) 8.0–10.2 cm, (d) 12.4–15.3 cm, and (e) 20.2–31.8 cm. The level of sound
pressure level is expressed in dB relative to 1 µPa (Vasconcelos and Ladich, 2008).

periods of development. The sounds of the carp fish
Codoma ornata reared in a complete isolation from the
eggs to an adult stage were in their acoustic parameters
the same as in individuals caught in nature and
emerged in the same behavioral situations (aggression,
courtship) (Johnston and Buchanan, 2007).
RANGE OF ACOUSTIC COMMUNICATION
Because of specific features of environment,
sounds in water can potentially distribute to large dis
tances. However, in shallow water bodies or in the off
shore where many vocalizing fish live, lowfrequency
acoustic signals damp far more rapidly and have a lim
ited zone of distribution. The range of acoustic signals
of fish depends not only on the depth, but also on the
pattern of the bottom ground and the physical struc
turization of the biotope, the presence in it of large
stones and rocks, stumps with root, vegetation, etc.
that not only hinder the distribution of acoustic waves,
but also, reflecting them, drastically complicate the
8 According to some early estimates, these strong
recognition of a valuable signal (Romanenko, 1974;
8 Reflection
of an acoustic wave in shallow waters occurs also
from the water and bottom surface.
Rogers and Cox, 1988; Forrest et al., 1993;
Kasumyan, 2005). Undoubtedly, maximum distance
at which reception or exchange with acoustic signals is
possible depends on the sound strength (acoustic pres
sure level) and the sensitivity of the auditory system of
a recipient.
There are few data on the distribution of fish
sounds in nature. It is found that the level of acoustic
pressure of sounds of Myripristis violaceus and
M. pralinus (frequency of 225 Hz) at the water body
depth of 5 m decreases by 10 dB already at 40 cm
(Horch and Salmon, 1973). Observations of fish
responses to sounds transmitted to water show that the
orientation to the sound source (underwater loud
speaker) does not occur at its removal for more than
3 m (Popper et al., 1973). Calculations performed for
Centrarchidae demonstrate that at a depth up to 1 m,
the sounds of these fish distribute for no more than 3–
4 m (Gerald, 1971).
The loudest sounds of the “boatwhistle” type
among fish are generated by males of Opsanus.
sounds completely damp at a distance of 10 m
(Tavolga, 1964). At an average depth of 1 m, the level
of acoustic pressure of inviting sounds of males of

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

1006 KASUMYAN

12

11 (a)

Pulse duration, cm
10

5 10 15 20 25 30
Body length, cm
1.2
(b)
log of the number of pulses

1.0

0.8

0.6

0.4

0.6 0.8 1.0 1.2 1.4 1.6

log of body length
145
(c)
140
Sound pressure level, dB

135
130
125
120
115
110

0.6 0.8 1.0 1.2 1.4 1.6

log of body length

Fig. 33. Dependence on body length of fish of (a) duration, the (b) number of acoustic pulses, and the (c) level of sound pressure
in an agonistic sound of the grunt type in Lusitanian toadfish Halobatrachus didactylus. The level of sound pressure level is
expressed in dB relative to 1 µPa (Vasconcelos and Ladich, 2008).

O. tau decreases by 18 dB already at a distance of 5 m tion varies from 3 to 9 dB/m, which is greater by six
9 orders of magnitude than in the ocean column), which
from the sound source. (The coefficient of consump limits acoustic communication to only several meters
9 Themost considerable decrease in the level of acoustic pressure
and explains a low development in these fish of audi
occurs at a distance of the first 1–2 m from the sound source tory sensitivity (Fine and Lenhardt, 1983). Boatwhis
(Fine and Lenhardt, 1983). tle sounds emitted by males of the Lusitanian toadfish

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

 ACOUSTIC SIGNALING IN FISH 1007

become slightly distinguishable at a distance of Number of behavioral

approximately 4 m (Fig. 35) (Amorim and Vasconce Number of sounds demonstrations
los, 2008). Sounds of males of these fish not only 30 30
attract females to the nest, but also signal other males 1
that the site is occupied. Since the nests of neighboring 25 2 25
males can be located close to each other (0.5 m and
less), it is obvious that such strong sounds are required, 20 20
firstly, for attracting females. It is likely that related to
it is a specific chorus singing of males when the invit 15 15
ing sounds of various males located not far from each
other follow each other up to 30 times per minute
10 10
(Amorim et al., 2006). Chorus singing considerably
increases the general acoustic background at the
5 5
spawning grounds of toadfish.
The sounds of males of Hawaiian dascyllus D. albi
sella lose their signal importance for females and other 5 4 3 2 1 0
individuals of the same species at a distance of more Number of days before spawning
than 11–12 m (Mann and Lobel, 1997). Considering
the seasonal and diurnal dynamics of sound genera Fig. 34. Change in (1) acoustic activity and (2) intensity of
tion and appearance of additional external noises of courtship behavior during 20 min in males of Tramitichro
various kinds related to sea disturbance state, wind, or mis intermedius in the prespawning period (Ripley and
Lobel, 2004).
rain, the listed estimates of distance of acoustic com
munication can change. In general, acoustic commu
nication in fish has a small range. The acoustic field (a)
formed around vocalizing fish in the offshore or in
shallow water bodies is limited to a radius of several
meters. In several cases, for instance, in males of
Pseudotropheus during courting a female, this distance
likely does not exceed several centimeters or 10–
Amplitude

20 cm (Simöes et al., 2008). Undoubtedly, far spread

(b)
ing sounds can unmask fish, attract predators, and,
thus, be contradaptive. Possibly this is why most fish
that are capable of producing specialized sounds and
using them for communication are found mainly at
sites where the distribution of sounds is limited. In the
pelagial where conditions for sound distribution are (c)
optimal, such fish are extremely few (Marshall, 1967).

CORRESPONDENCE OF ACOUSTIC SPECTRA 0.1 0.5 0.9 1.3 1.7

AND AUDITORY SENSITIVITY
The relationship between the capacity for sound
production and the development of auditory sensitiv
ity in fish is pronounced to different degrees. In some
species, for instance, in many Otophysi, these two
functions weakly correlate, which gives grounds to
suggest their independent evolutionary development
(Ladich, 1999, 2000). In other fish, primarily in those
that have no accessory auditory structures and that
cannot be related to auditory specialists, the corre
spondence between acoustic spectra and spectra of
auditory sensitivity is well pronounced. These fish
include Batrachoididae, Gobiidae, Pomacentridae,
Cichlidae, etc. For instance, in green damselfish Tra
mitichromis intermedius, sounds of males during court
ing a female are limited to a frequency range from 179
to 478 Hz that strictly corresponds to the range of fre
quencies of maximum auditory sensitivity of these
fish—200–500 Hz (Ripley et al., 2002). The ade
Time, s
Fig. 35. Oscillogram of a recording of the inviting sound of
the boatwhistle type emitted by males of Lusitanian toad
fish Halobatrachus didactylus recorded at different dis
tances from the underwater sound source: (a) 0.5, (b) 1.5,
and (c) 4.0 m (Amorim and Vasconcelos, 2008).
quately good coincidence of characteristics of audi
tory sensitivity and own sounds is observed also in
Pomacentridae, Mormyridae, and Osphronemidae
that use sounds during complex reproductive and ter
ritorial interactions (Myrberg and Spires, 1980; Craw
ford, 1993; Ladlich and Yan, 1998). For instance, in
green damselfish A. abdominalis, maximum amplitude
of sounds of aggression and sounds related to court
ship behavior is located in the zone of 100 to 400 Hz,
and the zone of the highest sensitivity to sounds is
located in the range of 95 to 240 Hz (Maruska et al.,
2007). These data indicate the coadaptation of sound

JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009

1008 KASUMYAN
generation and sound reception, as a result of which
fish are capable of efficiently interacting with each
other using acoustic signals. In general, because of the
absence in several fish of an obvious correspondence
between the frequency characteristics of acoustic sig
nals and the zones of maximum auditory sensitivity,
the issue of correlation between the development of
hearing and the capacity for sound production and the
width of the acoustic repertoire undoubtedly requires
study.
SOUNDS AND POLYMODAL
COMMUNICATION
Intraspecies communications in fish are exercised
owing to signals of different nature. The regulation of
complex behavioral forms in fish, as a rule, is provided
not by one stimulus, but by several stimuli perceived by
different sensory systems. For instance, in Mormy
ridae, in interrelations between the individuals of
opposite sexes in the spawning period, the electrore
ceptor and auditory systems well developed in these
fish play an important role. Electric signals generated
by these fish during spawning differ not only in differ
ent species, but also in mature females and males. The
communicative function of electric signals in fish is
obvious (Moller et al., 1979; Hopkins, 1981; Crawford
and Hopkins, 1989; Kramer, 1990). In response to
electric discharges of a female, males of Mormyridae
also exhibit courtship behavior and emit acoustic sig
nals distinguished by species and sexual specificts of
their structural and frequencyamplitude characteris
tics (Crawford, 1992; Crawford et al., 1997a). The
energy expenditures of fish related to generation of
acoustic signals are many times higher than in case of
electric signals (Crawford et al., 1997b). What is the
reason of the necessity or the biological importance of
sound generation in addition to specific and, hence,
highly informative electric signals? It was suggested
that electric signals, because of a small duration, less
than 100 µs, are difficult to recognize by fish (Hopkins
and Bass, 1981). However, it is difficult to agree with
such a hypothesis. The suggestion that acoustic signals
carry accessory information on the physical state and
sizes of males since sound generation is based on prin
ciples of mechanics looks more substantiated and true.
Owing to acoustic signals, females can choose larger
and stronger males among many pretenders (Craw
ford and Huang, 1999).
Playback to fish of recordings of their own sounds
is often terminated in the absence of any response to
these stimuli until an acoustic signal is accompanied
by simultaneous presentation of an accessory stimulus
of another nature, for instance, a visual stimulus
(Hawkins and Myrberg, 1983; Ladich, 1997). Another
example that well illustrates the importance of a poly
sensory provision of communications are results of
experiments performed at colonial bicolor damselfish
P. partitus. A successful defense of the personal terri
JOURNAL OF ICHTHYOLOGY
tory is possible only when its host generates in warning
visual and acoustic signals. Blocking of one of these
communication canals inevitably leads to the loss of
the site (Myrberg and Riggio, 1985; Myrberg, 1997).
Together with auditory, electric or visual stimuli,
the lateral line, tactile sense, and, undoubtedly, olfac
tory stimuli participate in the regulation of complex
behavioral forms. In the reproductive behavior, for
instance, using sex odors forming a complex of pre
and postovulatory pheromones of primer and release
types, a fine regulation of subsequent links of repro
ductive behavior is provided in all fish studied in this
respect without exception (Kasumyan, 2004). Inter
esting results were obtained due to comparative analy
sis of aggressive behavior and related to it sound gen
eration in Macropodus and Trichopsis. With reference
to these closely related fish it was established that the
more noticeable, diverse, and energetic demonstra
tion of visual signals of threat during fights, the less
actively and more seldom fish use acoustic stimuli. In
fish in which acoustic signaling is an obligatory and
well developed element of intraspecies fights, visual
demonstrations of threat are less pronounced (Bis
chof, 1996). Thus, the relative importance of stimuli of
different modalities in the regulation of complex forms
of behavior differs, even in fish similar in systematics
and behavior.
APPLIED ASPECTS
The ability to produce sounds was found in almost
1000 fish species, among them in many commercially
valuable fish—Gadidae, Clupeidae, Scianidae, etc.
Sounds emitted by some of them in the period of
acoustic activity are so strong that can be heard by the
naked ear of humans. This specific feature has been
long used by fishermen to discover aggregations of fish
such as, for instance, Argyrosomus regius—a large fish
distributed along the eastern coast of the Atlantic. In
order to discover sites of the drum concentration, fish
ermen, putting ear to the boat body, tried to perceive
sounds of these fish and, according to their strength,
choose a promising site for fishing (Lagardère and
Mariani, 2006). The same practice was used during
fishing of Sciaenidae by fishermen of Japan and China
(Takemura et al., 1978). Under modern conditions,
when the corresponding sound recording devices are
present, this mode of discovering fish, called passive
hydroacoustics, is very promising for use in the prac
tice of commercial fishery.
Owing to many doubtless advantages, the method
of passive acoustics attracts great attention for solving
different tasks, applied and scientific. This interest is
caused by the fact that potentially sounding fish due to
species specificity of sounds produced by them can be
discovered and observed. The identification of species
belonging, as well as the recognition of separate indi
viduals, are also possible. Undoubtedly such method
of tracing fish or separate individuals is less destructive
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
from the point of impact on fish and their environ
ment. Its use is not limited, for instance, by conditions
of water illumination or transparency, as is inherent to
methods of visual or video registration. Sound distri
bution to long distances makes it possible to perform a
distant tracing of fish, which reduces to minimum the
undesirable impact on them. Underwater sound
recording devices are relatively simple and not expen
sive, which is also an advantage of passive hydroacous
tics. The use of this method is not related to great time
expenditures, makes it possible to obtain necessary
evidence rather rapidly, and perform monitoring over
large water areas, including an autonomous regime.
During the last two decades, passive hydroacoustics
has undergone considerable development (Luczkovich
et al., 2008). The use of this method, for instance, for
discovering or specifying sites of fish distribution,
whose presence is difficult to reveal using other meth
ods, especially in large water bodies is very promising.
In this respect, an example of cuskeel O. marginatus is
interesting. It has been long considered that this small
coastal marine fish leading a nocturnal mode of life
and spending light hours of the day in the ground is
numerous in waters of the Atlantic to the south of New
York latitude. However, as was found, this is not so,
and this species is common also in northern waters.
This conclusion was made on the basis of underwater
listenings and discovery of typical spawning sounds of
cuskeel males in areas where previously this species
was not recorded (Rountree and BowersAltman,
2002). The registration of acoustic activity in fish
whose dynamics coincides in many species with the
reproduction period is used to determine the time of
the onset and termination of the spawning season
(Connaughton et al., 2002a) or to discover spawning
aggregations and to find spawning sites (Luczkovich
et al., 1999; Hawkins et al., 2002). For instance, the
use of passive hydroacoustics made it possible to estab
lish that haddock can form large spawning aggrega
tions not only in the open sea where, as was consid
ered, its spawning takes place, but also in the coastal
zone (Hawkins et al., 2002). Mapping of areas of
spawning of Sciaenidae in the estuary of the Savan
nach River performed on the basis of results of under
water listenings of sounds made it possible not only to
lay off at this place a navigational route with minimum
damage for fish, but also to assess the effect of bottom
deepening works on the reproduction of Sciaenidae in
this area (Ramcharitar et al., 2006). Using underwater
listening, the distribution of Sciaena umbra in the Gulf
of Trieste in the Adriatic Sea was elucidated, and it was
established that these relatively rare fish escaping, as
was considered previously, coastal sites where they can
be annoyed by humans, are most frequently found in
rocky piles near coastprotecting constructions, near
piers, berths, and in ports. Despite intensive naviga
tion, fish prefer to settle in such places because of a
large number of shelters suitable for them (Bonacito
et al., 2002).
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
1009
New types of hydrophones, sound recorders, and
software for analysis of recordings of fish sounds dras
tically increased the possibilities of passive hydroa
coustics during the last years (Luczkovich et al., 2008).
Due to modern devices, it is possible to record in
nature sounds of separate individuals of Bairdella
chrysoura at a distance to several hundreds of meters
(Sprague and Luczkovich, 2004). The aggregations of
vocalizing fish, such as B. chryosora, gray weakfish,
and some others were recorded at a distance to 1–2 km
(Luczkovich et al., 1999; D’Spain and Batchelor,
2006), and sounds of aggregations of Terapon theraps
were recorded at a distance of 5–8 km (McCauley and
Cato, 2000). In Norway, for monitoring of acoustic
activity in fish, autonomous stationary videoacoustic
platforms were elaborated that, in particular, are used
to study the spawning behavior of Atlantic cod and of
several other fish species (Rountree et al., 2003).
These possibilities open up new perspectives for
diverse studies of fish biology—behavior, distribution,
migrations, numbers, reproduction sites, monitoring
of the state of populations, etc.
One of the main problems hindering the develop
ment of passive hydroacoustics is an insufficient
amount of accumulated and significant data on fish
sounds, absence of systematized and accessible for a
wide circle of users of catalogues of digital records of
underwater sounds (Rountree et al., 2002). Available
for researchers are, as before, only two possible
approaches to obtaining data on species acoustic rep
ertoires: recordings of sounds generated by fish under
artificial conditions or the recording of such sounds in
a natural habitat, in situ. Both approaches have many
obvious limitations, and their use does not guarantee
obtaining inadequate results, for instance, because of
sound distortion and a complex acoustic background
in aquariums and basins or because of difficulties in
correlating a recorded sound in nature to its concrete
source or the conditions of its emergence. The use of
both approaches simultaneously permits receiving
more reliable results. It is also important to standard
ize the nomenclature (classification) of sounds and
their names, although it is difficult to achieve it
because of a complex range of sense associations and
their shades arising in researchers during listening of
sounds (Kasumyan, 2008).
The knowledge of fish sounds and those behavioral
situations in which they are generated or fish responses
to sounds permits the solution of practical tasks related
to aquculture. At fish farms, the visual observation of
the feeding activity of reared fish is often complicated
by a high stock density and water depth or turbidity. As
was found, there is a well pronounced relationship
between feeding and the intensity of sounds produced
by fish; therefore, it is possible to assess and control the
feeding activity of fish, analyzing the acoustic picture
in basins with cultivated fish. Special acoustic devices
are developed and suggested for these purposes
(Lagardère and Mallekh, 2000; Mallekh et al., 2003).
1010 KASUMYAN
A curious fact is reported that a significant stimulation
of growth of fish (carp Cyprinus carpio) can take place
when music is transmitted to basins with reared fish
(Vasantha et al., 2003).
Sounds can be efficient attractants and repellents
for fish, which is already long used by humans. In Rus
sia, fishermen for more than one century have used a
method of fishery of sheatfish Silurus glanis by “quok”
(Sabaneev, 1911); rhythmic blows on water with this
simple wooden device produce sounds that attract
sheatfish to the fishery site. This method until now
remains popular among amateur fishermen. Accord
ing to a long existing point of view, the attractive effect
of the “quok” sounds is explained by the fact that they
resemble sounds of frogs—one of favorite food items
of the sheatfish (Sabaneev, 1911). The “quok” sounds,
as their analysis demonstrated, represent pulses with
duration of approximately 130 ms and maximum fre
quency in the region of 270 Hz, and by the frequency,
the rhythm of pulses, and the general pattern resemble
sounds emitted by sheatfish during aggressivedefen
sive interactions (Sorokin and Simakov, 2004). The
results of other studies indicate the similarity of
“quok” sounds to sounds arising during feeding of the
sheatfish. Sounds emitted by “quok” so strongly excite
the sheatfish that it can jump onto the water surface
near a boat (Protasov, 1965). The justification of the
conclusion that the attracting action of the “quok”
sounds is based on the imitation of feeding sounds is
supported by data on maximum efficiency of such
fishing sheatfish in summer, while spawning in these
fish when concurrent and aggressive interactions can
aggravate occurs in spring.
There are diverse folk methods of attracting fish by
sounds, for instance, burbot Lota lota, river perch
P. fluviatilis, and others. Some of these methods used
presently and used before by fishermen of different
countries are listed in the monograph by Protasov
(1965). In recent years, modern acoustic attractants
have been developed, including for amateur fishery,
that represent devices transmitting to water sounds
that attract fish. For the purposes of pasture cultiva
tion, methods based on conditioned food reflexes to
sounds that formed in fish before their release for feed
ing into natural water bodies were developed.
Acoustic repellents are also promising for use for
different purposes. It is known that sharp sounds
whose intensity several times exceeds the background
level cause fright and flight in many sharks. Large
sharks are less perceptive to such sounds. The response
of some shark species Charcharinus falciformis to a
sharp sound is rather stable and can be repeated at
multiple repeated stimulations, while in sharks of
other species (C. longimanus), only the first one–two
presentations cause fright. Hammerhead shark
Sphyrna lewini usually flee sounds of even air bubbles
exhaled by scuba divers (Myrberg and Nelson, 1990).
Some fish are extremely sensitive to unexpected and
strong sounds and respond to them by sharp darts or
JOURNAL OF ICHTHYOLOGY
jumps, for instance, silver carp Hypophthalmichthys
molitrix or haarder Mugil cephalus. Such specific fea
ture of behavior of haarder was used by the Black Sea
fishermen for its discovery and fishing. Fishermen for
the fishery of freshwater fish used “botala”—wooden
rods with an empty metallic bank fixed at its end and
directed downwards. Sharp sounds arising during ver
tical blows with “botala” on water frightened fish,
which made net fishing more efficient (Protasov,
1965). Attempts are made to develop artificial acoustic
repellents imitating infrasounds arising during swim
ming of large predators and causing in fish an avoiding
response. The perspectivity of using generators of such
lowfrequency sounds for control of fish behavior
(Atlantic cod, Salmo salar, king salmon Oncorhynchus
tshawytscha, rainbow trout O. mykiss, and eel Anguilla
anguilla) was demonstrated not only during tests in
aquariums and basins, but also in natural water bodies
(Knudsen et al., 1992, 1997; Sand et al., 2000).
CONCLUSIONS
Acoustic signaling is important in behavior of
many fish. Using it, fish can find sites free for repro
duction and uniformly distribute over spawning
grounds, determine the presence of partners ready for
spawning, and choose among them those having the
highest reproductive potential. Owing to emitted
sounds, fish males not only attract females to them
selves, but also more efficiently protect their territory.
Species specificity of acoustic signals and differences
of fish in behavioral situations in which sounds are
generated promote the reproductive isolation of dwell
ing in common closely related fish. Acoustic signaling
permits synchronization spawning of genital products,
which is especially important for fish that spend not
more than several seconds on the spawning act. In
colonial fish, the generation of individually recog
nized sounds makes it possible not only to maintain
own site, but also to maintain the colony integrity.
In recent years, an obvious and rapid development
of studies of sounds and acoustic communication in
fish has been observed. Doubtless evidence of such
progress is not only a considerable number of special
and generalizing publications published during recent
years, but also the appearance of review papers con
cerning already not fish as a whole, but individual
orders or families of this most numerous group of ver
tebrate animals (see, for instance, Lobel, 2001; Fine
and Ladich, 2003; Ramcharitar et al., 2006). In books
devoted to sensory systems, behavior, and communi
cation in fish, sections dealing with hearing, sounds
and bioacoustics occupy a noticeable place (Ladich
et al., 2006). However, other animals—insects, birds,
and mammals are, as before, more comprehensively
studied in this respect (Zelick et al., 1999). Such lag
ging behind is accounted for by several reasons, the
main of which are technical difficulties in the registra
tion and analysis of sounds in an aquatic medium,
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
especially in small aquariums and basins. A complex
acoustic background and sound distortion observed
under such conditions were for a long time a serious
obstacle in the study of bioacoustics of fish and their
auditory characteristics. These specific features of
sounds also continue to hinder the development of
such studies also at the present time. Sound generation
by fish, as was shown on numerous examples above,
takes place only in definite situations related to repro
duction or complex intragroup relations. The genera
tion of conditions allowing fish to exhibit the corre
sponding behavior in an artificial situation, as well as
the observation of fish and recording of their activity in
natural water bodies are conjugated in most cases with
considerably greater efforts than those required in the
study of sounds of land animals.
As before, a quite noticeable imbalance between
the study of the soundgenerating apparatus and data
on the pattern of sounds emitted by fish and their pur
pose is observed. For instance, for Sciaenidae, Trigl
idae, and Batrachoididae—the most known groups of
sounding fish whose soundgenerating apparatus has
been well studied—there are few, as before, data on
the role of sounds and behavior, despite a secular his
tory of studies of sound generation in these fish
(Tower, 1908; Ramchritar et al., 2006). There are few
studies in which the signal importance of sounds gen
erated by fish is distinctly shown, especially in cases
when the acoustic repertoire is not limited to only one
type of sound. For many fish in which tympanic mus
cles were found, data on sounds emitted by them are
completely lacking. At the same time, for large groups
of fish, for instance, for Gobiidae, there are suffi
ciently much data on parameters of sounds generated
by them and the reasons of sound production; how
ever, the mechanism of sound generation remains
unclear. In fish emitting sounds, but having no tym
panic muscles, the presence of the stridulation method
of sound production is assumed, as a rule. However,
strict proofs of the justification of such suggestion or
description of a concrete stridulation mechanism are
absent in most cases. Special studies are required to
obtain such proofs.
The sounds produced by fish form the basis of the
natural acoustic background in water bodies. Accord
ing to studies performed in the area of the Great Bar
rier Reef, fish can cause a considerable increase in the
acoustic background in the sea (by 35 dB) (McCauley
and Cato, 2000). Drumming sounds produced by
Cynoscion xanthulus increase the noise level by 50 dB
(Fish and Cummings, 1972). It is noteworthy that it is
possible to identify underwater sounds with assurance
in exceptional cases. For instance, among a great
number of underwater sounds recorded in the area of
the Great Barrier Reef, the “species” belonging of the
sound source was determined for only one of them—
it was Therapon theraps (McCauley and Cato, 2000).
During underwater listening of sounds in different
sites of the Hudson River, 62 sound types were
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
1011
recorded; of them, the origin of only four sounds
caused no doubts; their sources were cuskeel O. mar
ginatum, O. tau, channel cat Ictalurus nebulosus, and
I. nebulosus. Among all sounds, 21 types were consid
ered biological by origin, and still 32 sounds could also
have such origin (Anderson et al., 2008). Because of
the poor study of visual acoustic repertoires of fish,
errors can arise during sound identification. For
instance, sounds of the “staccato” type that have been
long attributed to Prionotus carolinus and P. evolans
(Fish et al., 1952; Fish, 1954; Moulton,1958), actu
ally, as was established comparatively recently, are
emitted by cuskeel O. marginatum (Mann et al., 1997;
Sprague and Luczkovich, 2001). A certain confusion is
made by differences in terminology used by different
researchers in description of fish sounds.
The present concepts of evolution of sound gener
ation and acoustic communication, moving reasons of
their origin, and the relationship between sound gen
eration and presence in fish of accessory structures
increasing auditory sensitivity remain undoubtedly
weakly developed. Are the emergence in fish of sound
generation and an increase in auditory abilities always
two independent or weakly interrelated evolutionary
processes? New studies and analysis of available data
are needed to find an answer to this interesting and
important question.
The issue of what role, principal or auxiliary, is per
formed by sounds in fish behavior at reproduction,
protection of the territory, feeding, etc. is no less
important. Undoubtedly, such complex forms of
behavior should have a multisensory support, in which
the importance and biological sense of information
coming via different sensory canals will be different,
but mutually supplementing. It will be different in fish
differing in the mode of life and systematics and in
individuals of different ages or having different moti
vation states. There are extremely few such studies as
yet, but they demonstrate the importance, for
instance, of odor and visual stimuli when they affect
fish together with acoustic signals (Lugli et al., 2004;
Tricas et al., 2006).
The issue of the range of acoustic signals and the
sizes of an acoustic biological field created around
their source remains insufficiently studied. It becomes
increasingly more obvious that, in most sounding fish,
the information present in acoustic signals is trans
ferred over a relatively small distance. Are the small
sizes of an acoustic biological field related to those
limitations to distribution of acoustic oscillations that
exist in the offshore or at small depths where fish emit
ting sounds mainly dwell? It is known that sounds
unmask fish and attract predators to them, which
makes such fish more vulnerable. It was shown, for
instance, that bottlense dolphin feeding on fish, in
particular, Opsanus, finds according to sounds the sites
of their spawning aggregations, and then easily finds
an individual vocalizing prey from a distance of several
tens of meters (Gannon et al., 2005). In this respect,
1012 KASUMYAN
the unknown specific features of acoustic signaling in
fish inhabiting the ocean pelagial, especially meso
and bathypelagial where sound distribution is by many
orders of magnitude higher than in shallow waters are
extremely intriguing up to now.
Further progress in the study of sounds and acous
tic signaling will not only permit obtaining new knowl
edge on fish biology, their behavior, and communica
tion, but also will enable to develop new methods and
approaches in the study of fish and solve applied tasks
concerning fishery and cultivation and protection and
monitoring of the state of natural populations.
ACKNOWLEDGMENTS
I am grateful to workers of Moscow State Univer
sity—D.S. Pavlov and E.A. Marusov—who made
valuable remarks on the manuscript and to
T.V. Golovkina and L.S. Alekseeva for help in the manu
script layout. I am also grateful to foreign colleagues who
responded to the request to send copies of their publica
tions—W.N. Tavolga, A.D. Hawkins, M.C.P. Amorim,
A.H. Bass, J.D. Crawford, M.A. Connaughton,
M.L. Fine, F. Ladich, T.C. Tricas, E. Parmentier,
M. Lugli, S. Malavasi, D.A. Mann, and R. Rountree.
The study was supported in part by the Leading
Scientific Schools and Universities of Russia programs
of the Russian Foundation for Basic Research.
REFERENCES
1. V. C. Almada, M. C. P. Amorim, E. Pereira, et al.,
“Agonistic Behaviour and Sound Production in Gaid
ropsarus mediterraneus (Gadidae),” J. Fish. Biol. 49,
363–366 (1996).
2. M. C. P. Amorim, “Sound Production in the Blue
Green Damselfish Chromis viridis (Cuvier, 1830)
(Pomacentridae),” Bioacoustics 6, 265–272 (1996).
3. M. C. P. Amorim, “Diel and Seasonal Variations of
Sound Production in Captivity Grey Gurnards
Eutrigla gurnardus,” Acta Zool. Sinica 51 (6), 1013–
1022 (2005).
4. M. C. P. Amorim, “Diversity of Sound Production in
Fish,” in Communication in Fishes, Ed. by
V. I. F. Ladich, S. P. Collin, P. Moller, and
B. G. Kapoor (Science Publishers, Enfield, 2006),
Vol. 1, pp. 71–104.
5. M. C. P. Amorim and V. C. Almada, “The Outcome of
MaleMale Encounters Affects Subsequent Sound
Production during Courtship in the Cichlid Fish Ore
ochromis mossambicus,” Anim. Behav. 69, 595–601
(2005).
6. M. C. P. Amorim and A. D. Hawkins, “Crowling for
Food: Acoustic Emission During Competitive Feeding
of the Streaked Gurnard,” J. Fish. Biol. 57, 895–907
(2000).
7. M. C. P. Amorim and A. D. Hawkins, “Ontogeny of
Acoustic and Feeding Behaviour in the Grey Gurnard,
Eutrigla gurnardus,” Ethology 111, 255–269 (2005).
JOURNAL OF ICHTHYOLOGY
8. M. C. P. Amorim and A. S. M. Neves, “Acoustic Sig
naling During Courtship in the Painted Goby, Poma
toscistus pictus,” J. Mar. Biol. Ass. UK 87, 1017–1023
(2007).
9. M. C. P. Amorim and R. O. Vasconcelos, “Variability
in the Mating Calls of the Lusitanian Toadfish Halo
batrachus didactylus: Cues for Potential Individual
Recognition,” J. Fish. Biol. 73, 1267–1283 (2008).
10. M. C. P. Amorim, P. J. Fonseca, and V. C. Almada,
“Sound Production During and Spawning of Oreo
chromis mossambicus: MaleFemale and MaleMale
Interactions,” J. Fish. Biol. 62, 658–672 (2003).
11. M. C. P. Amorim, M. E. Knight, Y. Stratoudakis, and
G. F. Turner, “Differences in Sounds Made by Court
ing Males of Three Closely Related Lake Malawi
Cichlid Species,” J. Fish. Biol. 65, 1358–1371
(2004a).
12. M. C. P. Amorim, Y. Stratoudakis, and A. D. Hawkins,
“Sound Production during Competitive Feeding in the
Grey Gurnard,” J. Fish. Biol. 65, 182–194 (2004b).
13. M. C. P. Amorim, R. O. Vasconcelos, J. F. Marques,
and F. Almada, “Seasonal Variation of Sound Produc
tion in the Lusitanian Toadfish Halobatrachus didacty
lus,” J. Fish. Biol. 69, 1892–1899 (2006).
14. M. C. P. Amorim, J. M. Simóes, P. J. Fonseca, and
G. F. Turner, “Species Differences in Courtship
Acoustic Signals Among Five Lake Malawi Cichlid
Species (Pseudotropheus spp.),” J. Fish. Biol. 72,
1355–1368 (2008).
15. S. Amoser and F. Ladich, “Diversity in NoiseInduced
Temporary Hearing Loss in Otophysine Fishes,” J.
Acoust. Soc. Am. 113, 2170–2179 (2003).
16. S. Amoser and F. Ladich, “Are Hearing Sensitivity of
Freshwater Fish Adapted to the Ambient Noise in
Their Habitats?,” J. Exp. Biol. 208, 3533–3542
(2005).
17. S. Amoser and L. E. Wysocki, “Noise Emission Dur
ing the First Powerboat Race in an Alpine Lake and
Potentional Impact on Fish Communities,” J. Acoust.
Soc. Am. 116, 3789–3797 (2004).
18. S. Amoser, L. E. Wysocki, and F. Ladich, “Noise
Emission during the First Powerboat Race in an Alpine
Lake and Potentional Impact on Fish Communities,”
J. Acoust. Soc. Am. 116, 3789–3797 (2004).
19. K. A. Anderson, R. A. Rountree, and F. Juanes,
“Soniferous Fishes in Hudson River,” Trans. Am.
Fish. Soc. 137, 616–626 (2008).
20. S. B. Barber and W. H. Mowbray, “Mechanism of
Sound Production in the Sculpin,” Science 124
(3214), 219–220 (1956).
21. J. F. Barimo and M. L. Fine, “Relationship of Swim
Bladder Shape to the Directionality Pattern of Under
water Sound in the Oyster Toadfish,” Can. J. Zool. 76
(1), 134–143 (1998).
22. A. H. Bass, “Shaping Brain Sexuality,” Am. Sci. 84
(4), 352–363 (1996).
23. A. H. Bass and R. Baker, “Evolution of Homologous
Vocal Control Traits,” Brain Behav. Evol. 38, 240–254
(1991).
24. A. H. Bass, D. A. Bodnar, and M. A. Marchaterre,
“Complementary Explanations for Existing Pheno
types in Acoustic Communication System,” in The
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
Design of Animal Communication, Ed. by M.D. Hauser
and M. Konishi (MIT Press, Cambridge, MA, 1999),
pp. 493–514.
25. B. Bergert and P. C. Wainwright, “Morphology and
Kinematics of Prey Capture in the Syngnathid Fishes
Hippocampus erectus and Syngnathus floridae,” Mar.
Biol. (Berlin) 127, 563–570 (1997).
26. C. Bischof, “Diversity in Agonistic Behavior of Croak
ing Gouramis (Trichopsis vittata, T. schalleri, and
T. pumpila; Anabantoidei) and the Paradise Fish
(Macropodus opercularis, Anabantoidei),” Aggressive
Behav. 22 (6), 447–455 (1996).
27. C. Bonacito, M. Costantini, M. Picciulin, et al., “Pas
sive Hydrophone Census of Sciaena umbra (Sci
aenidae) in the Gulf of Trieste (Northern Adriatic Sea,
Italy),” Bioacoustics 12 (2–3), 292–294 (2002).
28. P. R. Boudreau, “Acoustic Observations of Patterns of
Aggregation in Haddock (Melanogrammus aeglefinus)
and Their Significance to Production and Catch,”
Can. J. Fish. Aquat. Sci. 49, 23–31 (1992).
29. R. K. Brantley and A. H. Bass, “Alternative Male
Spawning Tactics and AcousticSignals in the Plainfin
Midshipman Fish Porichthys notatus Girard (Teleostei,
Batrachoididae),” Ethology 96, 213–232 (1994).
30. V. M. Brawn, “Reproduction Behaviour of the Cod
Gadus callarias (L.),” Behaviour 18, 177–197 (1961a).
31. V. M. Brawn, “Sound Production by the Cod Gadus
callarias (L.),” Behaviour 18, 239–255 (1961b).
32. C. M. Breder, Jr., “Seasonal and Diurnal Occurrences
of Fish Sounds in a Small Florida Bay,” Bull. Am.
Mus. Natur. Hist. 138, 325–378 (1968).
33. A. A. Bremner, E. A. Trippel, and J. H. Terhune,
“Sound Production by Adult Haddock, Melanogram
mus aeglefinus, in Isolation, Pairs, and Trios,” Envi
ron. Biol. Fishes 65, 359–362 (2002).
34. R. M. Bruch and F. P. Binkowski, “Spawning Behavior
of Lake Sturgeon (Acipenser fulvescens),” J. Appl. Ich
thyol. 18, 570–579 (2002).
35. K. C. Chen and H. K. Mok, “Sound Production in the
Anemonefishes, Amphiprion clarkia and A. frenatus
(Pomacentridae) in Captivity,” Jpn. J. Ichthyol. 35,
90–97 (1988).
36. P. L. Colin, “Daily and SummerWinter Variation in
Mass Spawning of the Stripped Parrotfish, Scarus cro
icensus,” U.S. Fish Bull. 76, 117–124 (1978).
37. D. J. Colson, S. N. Patek, L. Brainerd, and
S. M. Lewis, “Sound Production During Feeding in
Hyppocampus Seahorses (Sygnathidae),” Environ.
Biol. Fishes 51, 221–229 (1998).
38. Communication in Fihes, Vols. 1–2, Ed. by F. Ladich,
S. Collin, P. Moller, and B. G. Kapoor (Sci. Publ.,
Einfield, 2006).
39. M. A. Connaughton, “Sound Generation in the Sea
Robin (Prionotus carolinus), a Fish with Alternate
Sonic Muscle Contraction,” J. Exp. Biol. 207, 1643–
1654 (2004).
40. M. A. Connaughton and M. H. Taylor, “Seasonal
Cycles in Sonic Muscles of the Weakfish, Cynoscion
Regalis,” U.S. Fish. Bull. 92, 697–703 (1994).
41. M. A. Connaughton and M. H. Taylor, “Seasonal and
Daily Cycles in Sound Production Associated with
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
1013
Spawning in the Weakfish, Cynoscion regalis,” Envi
ron. Biol. Fishes 42, 233–240 (1995).
42. M. A. Connaughton and M. H. Taylor, “Drumming,
Courtship, and Spawning Behavior in Captive Weak
fish, Cynoscion regalis,” Copeia, No. 1, 195–199
(1996).
43. M. A. Connaughton, M. L. Fine, and M. H. Taylor,
“The Effects of Seasonal Hypertrophy and Atrophy on
Fiber Morphology, Metabolic Substrate Concentra
tion and Sound Characteristics of the Weakfish Sonic
Muscle,” J. Exp. Biol. 200, 2449–2457 (1997).
44. M. A. Connaughton, M. H. Taylor, and M. L. Fine,
“Effects of Fish Size and Temperature on Weakfish
Disturbance Calls: Implications for the Mechanism of
Sound Generation,” J. Exp. Biol. 203, 1503–1512
(2000).
45. M. A. Connaughton, M. L. Fine, and M. H. Taylor,
“Use of Sound for Localization of Spawning Weakfish
in Delaware Bay (USA) and Effects of Fish Size, Tem
perature and Season on Sound Parameters,” Bioa
coustics 12 (2–3), 294–296 (2002a).
46. M. A. Connaughton, M. L. Fine, and M. H. Taylor,
“Weakfish Sonic Muscle: Influence of Size, Tempera
ture and Season,” J. Exp. Biol. 205, 2183–2188
(2002b).
47. J. D. Crawford, “Sex Recognition by Electric Cues in
a SoundProducing Mormyrid Fish, Pollimyrus isi
dori,” Brain Behav. Evol. 38, 20–38 (1991).
48. J. D. Crawford, “Individual and Sex Specificity in the
Electric Organ Discharges of Breeding Mormyrid Fish
(Pollimyrus isidori),” J. Exp. Biol. 164, 79–102 (1992).
49. J. D. Crawford, “Central Auditory Neurophysiology
of a SoundProducing Fish: The Mesencephalon of
Pollimyrus isidori (Mormyridae),” J. Comp. Physiol. A
172, 139–152 (1993).
50. J. D. Crawford, “Hearing and Acoustic Communica
tion in Mormyrid Electric Fishes,” Mar. Freshwater
Behav. Physiol. 29, 65–86 (1997a).
51. J. D. Crawford, “FeatureDetecting Auditory Neu
rons in the Brain of a SoundProducing Fish,” J.
Comp. Physiol. A 180, 439–450 (1997b).
52. J. D. Crawford and C. D. Hopkins, “Detection of a
Previously Unrecognized Mormyrid Fish (Mormyrus
subundulatus) by Electric Discharge Characters,”
Cybium 13, 319–326 (1989).
53. J. D. Crawford and X. Huang, “Communication Sig
nals and Sound Production Mechanisms of Mormyrid
Electric Fish,” J. Exp. Biol. 202, 1417–1426 (1999).
54. J. D. Crawford, M. Hagedorn, and C. D. Hopkins,
“Acoustic Communication in an Electric Fish, Pol
limirus isidori (Mormyridae),” J. Comp. Physiol. A
159, 297–310 (1986).
55. J. D. Crawford, A. P. Cook, and A. S. Heberlein, “Bio
acoustic Behavior of African Fishes (Mormyridae):
Potential Cues for Species and Individual Recognition
in Pollimyrus,” J. Acous. Soc. Am. 102, 1200–1212
(1997a).
56. J. D. Crawford, P. Jacob, and V. Benech, “Sound Pro
duction and Reproductive Ecology of Strongly Acous
tic Fish in Africa: Pollimyrus isidori, Mormyridae,”
Behaviour 134, 677–725 (1997b).
1014 KASUMYAN
57. W. C. Cummings, B. D. Brachy, and W. F. Hernkind,
The Occurrence of Underwater Sounds of Biological Ori
gin of the West Coast of Birnini, Bahamas (1964).
58. L. S. Demski, J. W. Gerald, and A. N. Popper, “Cen
tral and Peripheral Mechanisms of Teleost Sound Pro
duction,” Am. Zool. 13, 1141–1167 (1973).
59. T. M. Dmitrieva and V. A. Ostroumov, Sex Pheromones
and Reproductive Behavior of Fish (Irkutskii Univer
sitet, Irkutsk, 1992) [in Russian].
60. M. E. Dos Santos, T. Modesto, R. J. Matos, et al.,
“Sound Production by the Lusitanian Toadfish, Halo
batrachus didactylus,” Bioacoustics 10, 309–321
(2000).
61. G. L. D’Spain and H. H. Batchelor, “Observations of
Biological Choruses in the Southern California Bight:
A Chorus at Midfrequencies,” J. Acoust. Soc. Am.
120, 1940–1955 (2006).
62. M. Dufossé, “Recherches sur les Bruits et les Sons
Expressifs Quefout Untend des Poisons d’Europe,”
Ann. Sci. Nature. Zool. Biol., Ser. 5 19, 1–53 (1874).
63. D. J. Dunning, Q. E. Ross, O. Geoghegan, et al., “Ale
wives Avoid HighFrequency Sound,” N. Am. J. Fish.
Management 12, 407–416 (1992).
64. F. Engen and I. Folstad, “Cod Courtship Song: A Song
at the Expense of Dance?,” Can. J. Zool. 77 (4), 542–
550 (1999).
65. P. S. Enger, “Frequency Discrimination in Teleosts:
Central or Peripheral?,” in Hearing and Sound Com
munication in Fishes, Ed. by W. N. Tavolga, A. N. Pop
per, and R. R. Fay (Springer, Berlin, 1981), pp. 243–
255.
66. P. S. Enger, A. J. Kalmijn, and O. Sand, “Behavioral
Identification of Lateral Line and Inner Ear Func
tion,” in The Mechanosensory Lateral Line: Neurobiol
ogy and Evolution, Ed. by S. Coombs, D. Görner, and
H. Münz (Springer, New York, 1989), pp. 575–590.
67. J. J. Feher, T. D. Waybright, and M. L. Fine, “Com
parison of Sarcoplasmic Reticulum Capabilities in
Toadfish (Opsanus tau) Sonic Muscle and Rat Fast
Twitch Muscle,” J. Muscle Res. Cell Motil. 19, 661–
674 (1998).
68. M. L. Fine, “Seasonal and Geographic Variation of
the Mating Call of the Oyster Toadfish Opsanus tau,”
Oecologia 36, 45–57 (1978).
69. M. L. Fine and F. Ladich, “Sound Production, Spine
Locking, and Relted Adaptations,” in Catfishes, Ed. by
G. Arratia, B. G. Kapoor, M. Chardon, and M. Diego
(Science Publisher, Enfield, 2003), Vol. 1, pp. 249–
290.
70. M. L. Fine and M. L. Lenhardt, “ShallowWater
Propagation of the Toadfish Mating Call,” Comp.
Biochem. Physiol. A. 76, 225–231 (1983).
71. M. L. Fine, H. E. Winn, and B. L. Olla, “Communi
cation in Fishes,” in How Animals Communicate, Ed.
by T. A. Sebeok (Indiana Univ., Bloomington, 1977).
72. M. L. Fine, D. McElroy, J. Rafi, et al., “Lateralization
of Pectoral Stridulation Sound Production in the
Channel Catfish,” Physiol. Behav. 60, 753–757
(1996).
73. J. L. Finstad and J. T. Nordeide, “Acoustic Repertoire
of Spawning Cod, Gadus morhua,” Environ. Biol.
Fishes 70, 427–433 (2004).
JOURNAL OF ICHTHYOLOGY
74. J. F. Fish, “The Effect of Sound Playback on the Toad
fish,” in Behavior of Marine Animals: Current Perspec
tives in Research. Vol. 2: Vertebrates, Ed. by H. E. Winn
and B. L. Olla (Pergamon Press, New York, 1972),
pp. 386–434.
75. J. F. Fish and W. C. Cummings, “A 50dB Increase in
Sustained Ambient Noise from Fish (Cynoscion xan
thulus),” J. Acoust. Soc. Am. 52, 1266–1270 (1972).
76. M. Fish, “The Character and Significance of Sound
Production Among Fishes of the Western North
Atlantic,” Bull. Bingham Oceanogr. Collect. 14 (3),
1–109 (1954).
77. M. Fish, Biological Sources of Continuous Surrounding
Sea Noises, in Marine Bioacoustics, Ed. by
U. N. Tavolga (Sudostroenie, Leningrad, 1969).
78. M. P. Fish and W. H. Mowbray, Sounds of Western
North Atlantic Fishes (John Hopkins Univ. Baltimore,
1970).
79. M. P. Fish, A. S. Kelsey, and W H. Mowbray, “Studies
on the Production of Underwater Sound by North
Atlantic Coastal Fishes,” J. Mar. Res. 11, 180–193
(1952).
80. T. G. Forrest, G. L. Miller, and J. R. Zagar, “Sound
Propagation in Shallow Water: Implications for
Acoustic Communication by Aquatic Animals,” Bioa
coustics 4, 259–270 (1993).
81. E. Forsgren, “Mate Sampling in a Population of Sand
Gobies,” Anim. Behav. 53, 267–276 (1997).
82. D. P. Gannon, N. B. Barros, D. P. Nowacek, et al.,
“Prey Detection by Bottlenose Dolphins (Tursiops
truncatus): An Experimental Test of the Passive Listen
ing Hypothesis,” Anim. Behav. 69, 709–720 (2005).
83. J. W. Gerald, “Sound Production During Courtship in
Six Species of Sunfish (Centrarchidae),” Evolution
25, 75–87 (1971).
84. R. G. Gilmore, “Sound Production and Communica
tion in the Spotted Seatrout,” in Biology of Spotted
Seatrout, Ed. by S. A. Bortone (CRC Press, Boca
Raton, Florida, 2003), pp. 177–195.
85. G.A. Gray and H. E. Winn, “Reproductive Ecology
and Sound Production of the Toadfish, Opsanus tau,”
Ecology 42, 274–282 (1961).
86. A. M. Gronell, “Visiting Behavior by Female of the
Sexually Dichromatic Damselfish, Chrysiptera cyanea
(Teleostei: Pomacentridae): A Probable Method of
Assessing Male Quality,” Ethology 81, 89–122 (1989).
87. W. C. Guest and J. L. Lasswell, “A Note of Courtship
Behavior and Sound Production of Red Drum,”
Copeia, No. 2, 337–338 (1978).
88. M. C. Hastings, A. N. Popper, J. J. Finneran, and
P. J. Landford, “Effects of Lowfrequency Underwater
Sound on Hair Cells of the Fish Astronotus ocellatus,”
J. Acoust. Soc. Am. 99, 1759–1766 (1996).
89. A. D. Hawkins and M. C. P. Amorim, “Spawning
Sounds of the Male Haddock, Melanogrammus aeglefi
nus,” Environ. Biol. Fishes 59, 29–41 (2000).
90. A. D. Hawkins and A. A. Myrberg, “Hearing and
Sound Communication Underwater,” in Bioacoustics,
a Comparative Approach, Ed. by B. Lewis (Academic
Press, London, 1983), pp. 347–405.
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
91. A. D. Hawkins and K. J. Rasmussen, “The Sound of
Gadoid Fish,” J. Mar. Biol. Ass. U. K 58, 891–911
(1978).
90. A. D. Hawkins, K. J. Chapman, and D. J. Symonds,
“Spawning of Haddock in Captivity,” Nature 215,
923–925 (1967).
92. A. D. Hawkins, L. Casaretto, M. Picciulin, and
K. Olsen, “Locating Spawning Haddock by Means of
Sound,” Bioacoustics 12 (2–3), 284–286 (2002).
93. S. M. Henglmüller and F. Ladich, “Development of
Agonistic Behaviour and Vocalization in Croaking
Guramis,” J. Fish. Biol. 54 (2), 380–395 (1999).
94. D. M. Higgs, “Auditory Cues As Ecological Signals for
Marine Fishes,” Mar. Ecol.: Proc. Ser. 285, 213–222
(2005).
95. C. D. Hopkins, “On the Diversity of Electric Signals
on a Community of Mormyrid Electric Fish in West
Africa,” Am. Zool. 21, 211–222 (1981).
96. C. D. Hopkins and A. H. Bass, “Temporal Coding of
Species Recognition Signals in an Electric Fish,” Sci
ence 212, 85–87 (1981).
97. K. Horch and M. Salmon, “Adaptations to the Acous
tic Environment by the Squirrelfishes Myripristis viola
ceus and M. pralinus,” Mar. Behav. Physiol. 2, 121–
139 (1973).
98. J. A. Hutchings, T. D. Bishop, and C. R. McGregor
Shaw, “Spawning Behaviour of Atlantic Cod, Gadus
morhua: Evidence of Mate Competition and Mate
Choice in a Broadcast Spawner,” Can. J. Fish. Aquat.
Sci. 56, 97–104 (1999).
99. R. M. Ibara, L. T. Penny, A. W. Ebeling, et al., “The
Mating Call of the Plainfin Midshipman Fish Porich
thys notatus,” in Predators and Prey in Fishes, Ed. by
D. L. G. Noakes, D. G. Lindquist, G. S. Helfman,
and J. A. Ward (Junk Publ., the Hague, 1983),
pp. 205–212.
100. P. L. James and K. L. Heck, Jr., “The Effects of Habi
tat Complexity and Light Intensity on Ambush Preda
tion within a Simulated Seagrass Habitat,” J. Exp.
Mar. Biol. Ecol. 176, 187–200 (1994).
101. D. L. Johnson, “Sound Production in Cyprinodon
bifasciatus (Cyprinodontiformes),” Environ. Biol.
Fishes 59, 341–346 (2000).
102. C. E. Johnston and H. M. Buchanan, “Learned or
Innate Production of Acoustic Signals in Fishes: A
Test Using a Cyprinid,” Environ. Biol. Fishes 78,
183–187 (2007).
103. C. E. Johnston and D. L. Johnston, “Sound Produc
tion During the Spawning Season in CavityNesting
Darters of the Subgenus Catonotus (Percidae: Etheo
stoma),” Copeia, No. 2, 475–481 (2000a).
104. C. E. Johnston and D. L. Johnston, “Sound Produc
tion in Pimephales notatus (Rafinesque) (Cyprin
idae),” Copeia, No. 2, 567–571 (2000b).
105. C. E. Johnston and C. T. Phillips, “Sound Production
in Sturgeon Scaphirhynchus albus and S. platorynchus
(Acipenseridae),” Environ. Biol. Fishes 68, 59–64
(2003).
106. C. E. Johnston and S. P. Vives, “Sound Production in
Codoma ornate (Girard) (Cyprinidae),” Environ. Biol.
Fishes 68, 81–85 (2003).
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11
1015
107. C. E. Johnston, M. K. Bolling, D. E. Holt, and
C. T. Phillips, “Production of Acoustic Signals During
Aggression in Coosa Bass, Micropterus coosae,” Envi
ron. Biol. Fishes 82, 17–20 (2008).
108. A. O. Kasumyan, “Behavioral Response of Male Aci
penserids to a Releasing Postovulatory Sex Pheromone
of Females,” Dokl. Akad. Nauk 333 (3), 402–404
(1993).
109. A. O. Kasumyan, “The Lateral Line in Fish: Structure,
Function, and Role in Behavior,” J. Ichthyol. 43
(Suppl. 2), S175–S213 (2003).
110. A. O. Kasumyan, “The Olfactory System in Fish:
Structure, Function, and Role in Behavior,” J. Ich
thyol. 44 (Suppl. 2), S180–S223 (2004).
111. A. O. Kasumyan, “Structure and Function of Auditory
System in Fish,” J. Ichthyol. 45 (Suppl. 2), S223–
S270 (2005).
112. A. O. Kasumyan, “Sounds and Sound Production in
Fishes,” J. Ichthyol. 48 (11), 981–1030 (2008).
113. T. N. Kenyon, “The Significance of Sound Intercep
tion to Males of the Bicolor Damselfish Pomacentrus
partitus During Courtship,” Environ. Biol. Fishes 40,
391–405 (1994).
114. F. Kirschbaum, K. L. Tolstoganova, and P. Williot,
“Acoustic Activity of Large Juvenile American Atlantic
Sturgeon, Acipenser oxyrhinchus, and Western Euro
pean Sturgeon, Acipenser sturio,” in Technical Com
pendium, Proc. 4th Int. Symp. on Sturgeon (2001),
p. 37.
115. R. A. Knapp and J. T. Kovach, “Courtship as an Hon
est Indicator of Male Parental Quality in the Bicolor
Damselfish, Segastes partitus,” Behav. Ecol. 2, 295–
300 (1991).
116. F. R. Knudsen, P. S. Enger, and O. Sand, “Awareness
Reactions and Avoidance Responses to Sound in Juve
nile Atlantic Salmon, Salmo salar,” J. Fish. Biol. 40,
523–534 (1992).
117. F. R. Knudsen, C. B. Schreck, S. M. Knapp, et al.,
“Infrasound Produces Flight and Avoidance Responses
in Pacific Juvenile Salmonids,” J. Fish. Biol. 51, 824–
829 (1997).
118. B. Kramer, Electrocommunication in Teleost Fishes:
Behavior and Experiments (Springer, Blackwell Sci.
Publ., Berlin, 1990).
119. J. Krause and G. D. Ruxton, Living in Groups (Oxford
Univ. Press, New York, 2002).
120. F. Ladich, “Sound Production by the Dudgeon Gobio
gobio (a Common European Freshwater Fish (Cyprin
idae, Teleostei),” J. Fish Biol. 32, 707–715 (1988).
121. F. Ladich, “Sound Production by the River Bullhead
Cottus gobio (Cottidae, Teleostei),” J. Fish Biol. 35,
531–538 (1989).
122. F. Ladich, “Comparative Analysis of Swimbladder
(Drumming) and Pectoral (Stridulation) Sounds in
Three Families of Catfishes,” Bioacoustics 8, 85–208
(1997).
123. F. Ladich, “Did Auditory Sensitivity and Vocalization
Evolve Independently in Otophysan Fishes?,” Brain
Behav. Evol. 53, 288–304 (1999).
2009
1016 KASUMYAN
124. F. Ladich, “Acoustic Communication and the Evolu
tion of Hearing in Fishes,” Philos. Trans. Roy. Soc.
Lond. B 355, 1285–1288 (2000).
125. F. Ladich, “Sound Production and Acoustic Commu
nication,” in The Senses of Fish. Adaptations for the
Reception of Natural Stimuli, Ed. by G. Von Der Emde,
J. Mogdans, and B. G. Kapoor (New DehliHeidel
berg, Narosa, 2004), pp. 210–230.
126. F. Ladich and A. Myrberg, Jr., “Agonistic Behavior and
Acoustic Communication,” in Communication in
Fishes, Ed. by F. Ladich, S. P. Collin, P. Moller, and
B. G. Kapoor (Sci. Publ., Enfield, 2006), Vol. 1,
pp. 121–148.
127. F. Ladich and A. Tadler, “Sound Production in
Polypterus (Osteichthys: Polypteridae),” Copeia,
No. 4, 1076–1077 (1988).
128. F. Ladich and H. Y. Yan, “Correlation between Audi
tory Sensitivity and Vocalization in Anabantoid
Fishes,” J. Comp. Physiol. A. 182, 737–746 (1998).
129. F. Ladich, C. Bischof, G. Schleinzer, and A. Fuchs,
“Intra and Interspecific Differences in Agonistic
Vocalization in Croaking Gouramis (Genus: Trichop
sis, Anabantoidei, Teleostei),” Bioacoustics 4, 131–
141 (1992a).
130. F. Ladich, W. Brittinger, and H. Kratochvil, “Signifi
cance of Agonistic Vocalization in the Croaking
Gourami (Trichopsis vittatus, Teleostei),” Ethology 90
(4), 307–314 (1992b).
131. J. P. Lagardére and R. Mallekh, “Feeding Sounds of
Turbot (Scophthalmus maximus) and Their Potential
Use in the Control of Food Supply in Aquaculture.
I. Spectrum Analysis of the Feeding Sounds,” Aquac
ulture 189 (3–4), 251–258 (2000).
132. J. P. Lagardére and A. Mariani, “Spawning Sounds in
Meagre Argyrosomus regius Recorded in the Gironda
Estuary, France,” J. Fish. Biol. 69, 1697–1708 (2006).
133. J. P. Lagardére, R. Mallekh, and A. Mariani, “Acoustic
Characteristics of Two Feeding Modes Used by Brown
Trout (Salmo trutta), Rainbow Trout (Oncorhynchus
mykiss), and Turbot (Scophthalmus maximus),”
Aquaculture 240 (1–4), 607–614 (2004).
134. M. Lamml and B. Kramer, “Sound Production in the
Reproductive Behaviour of the Weakly Electric Fish
Pollimyrus marianne Kramer et al., 2003 (Mormy
ridae, Teleostei),” Bioacoustics 15, 51–78 (2005).
135. M. Lamml and B. Kramer, “Differentiation of Court
ship Songs in Parapatric Sibling Species of Dwarf
Stonebashers from Southern Africa (Mormyridae,
Teleostei),” Behaviour 143, 783–810 (2006).
136. K. Lindström, “Female Spawning Patterns and Male
Mating Success in the Sand Goby Pomatoschistus
minutus,” Mar. Biol. (Berlin) 113, 475–480 (1992).
137. K. Lindström and M. Lugli, “A Quantitative Analysis
of the Courtship Acoustic Behaviour and Sound Pat
terning in Male Sand Goby, Pomatoschistus minutus,”
Environ. Biol. Fishes 58, 411–424 (2000).
138. P. S. Lobel, “Sounds Produced by Spawning Fishes,”
Environ. Biol. Fishes 33, 351–358 (1992).
139. P. S. Lobel, “Possible Species Specific Courtship
Sounds by Two Sympatric Fishes in Lake Malawi,
Africa,” Environ. Biol. Fishes 52, 443–452 (1998).
JOURNAL OF ICHTHYOLOGY
140. P. S. Lobel, “Courtship Sounds of the Pacific Dam
selfish, Abudefduf sordidus (Pomacentridae),” Biol.
Bull. 197, 243–244 (1999).
141. P. S. Lobel, “Acoustic Behavior of Cichlid Fishes,” J.
Aquacult. Aquat. Sci. 9, 89–108 (2001).
142. P. S. Lobel and D. A. Mann, “Spawning Sounds of the
Damselfish, Dascyllus albisella (Pomacentridae) and
Relationship to Male Size,” Bioacoustics 6, 187–198
(1995).
143. K. E. Loesser, J. Rafi, and M. L. Fine, “Embryonic,
Juvenile, and Adult Development of the Toadfish
Sonic Muscle,” Anat. Rec. 249, 469–477 (1997).
144. J. J. Luczkovich, M. W. Sprague, S. E. Johnson, and
R. C. Pullinger, “Delimiting Spawning Areas of Weak
fish, Cynoscion regalis (Family Sciaenidae), in Pamlico
Sound, North Carolina Using Passive Hydroacoustic
Surveys,” Bioacoustics 10, 143–160 (1999).
145. J. J. Luczkovich, H. J. Daniel, M. Hutchinson, et al.,
“Sound of Sex and Death in the Sea: Bottlenose Dol
phin Whistles Suppress Mating Choruses of Silver
Perch,” Bioacoustics 10, 323–334 (2000).
146. J. J. Luczkovich, D. A. Mann, and R. A. Rountree,
“Passive Acoustics as a Tool in Fishery Science,”
Trans. Am. Fish. Soc. 137, 533–541 (2008).
147. M. Lugli and P. Torricelli, “Prespawning Sound Pro
duction in Mediterranean SandGobies,” J. Fish.
Biol. 54, 691–694 (1999).
148. M. Lugli, L. Bobbio, P. Torricelli, and G. Gandolfi,
“Breeding Ecology and Male Spawning Success in
Two HillStream Populations of Freshwater Goby,
Padogobius martensii,” Environ. Biol. Fishes 35, 37–
48 (1992).
149. M. Lugli, G. Pavan, P. Torricelli, and L. Bobbio,
“Spawning Vocalizations in Male Freshwater Gobiids
(Pisces, Gobiidae),” Environ. Biol. Fishes 43, 219–
231 (1995).
150. M. Lugli, P. Torricelli, G. Pavan, and P. J. Millder,
“Breeding Sounds of Male Padogobius nigricans with
Suggestions for Further Evolutionary Study of Vocal
Behaviour in Gobioid Fishes,” J. Fish. Biol. 49, 648–
657 (1996).
151. M. Lugli, P. Torricelli, G. Pavan, and D. Mainardi,
“Sound Production during Courtship and Spawning
Among Freshwater Gobiids (Pisces, Gobiidae),” Mar.
Fresh. Behav. Physiol 29, 109–126 (1997).
152. M. Lugli, H. Y. Yan, and M. L. Fine, “Acoustic Com
munication in Two Freshwater Gobies: The Relation
ship Between Ambient Noise, Hearing Thresholds and
Sound Spectrum,” J. Comp. Physiol. A 189, 309–320
(2003).
153. M. Lugli, G. Pavan, and P. Torricelli, “The Response
of the Male Freshwater Goby to Natural and Synthetic
Male Courtship Sound Playback Following Exposure
to Different Female Sexual Stimuli,” Ethol. Ecol.
Evol. 16, 55–70 (2004).
154. S. Malavasi, P. Torricelli, M. Lugli, et al., “Male
Courtship Sounds in a Teleost with Alternative Repro
ductive Tactics, the Grass Goby, Zosterisessor ophio
cephalus,” Environ. Biol. Fishes 66, 231–236 (2003).
155. R. Mallekh, J. P. Lagardére, J. P. Eneau, and C. Clou
tour, “An Acoustic Detector of Turbot Feeding Activ
ity,” Aquaculture 221 (1–4), 481–489 (2003).
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
156. D. A. Mann and P. S. Lobel, “Passive Acoustic Detec
tion of Sound Produced by the Damselfish Dascyllus
albisella (Pomacentridae),” Bioacoustics 6, 199–213
(1995).
157. D. A. Mann and P. S. Lobel, “Propagation of Damself
ish (Pomacentridae) Courtship Sounds,” J. Acoust.
Soc. Am. 101 (6), 3783–3791 (1997).
158. D. A. Mann and P. S. Lobel, “Acoustic Behavior of the
Damselfish Dascyllus albisella: Behavioral and Geo
graphic Variation,” Environ. Biol. Fishes 51, 421–428
(1998).
159. D. A. Mann, J. BowersAltman, and R. A. Rountree,
“Sounds Produced by the Striped CuskEel Ophidion
marginatum (Ophidiidae) during Courtship and
Spawning,” Copeia, No. 3, 610–612 (1997).
160. D. A. Mann, B. M. Casper, K. S. Boyle, and
T. C. Tricas, “On the Attraction of Larval Fishes to
Reef Sounds,” Mar. Ecol.: Proc. Ser. 338, 307–310
(2007).
161. N. B. Marshall, “SoundProducing Mechanisms and
the Biology of DeepSea Fishes,” in Marine Bio
Acoustics, Ed. by W. N. Tavolga (Pergamon Press,
Oxford, 1967), pp. 123–133.
162. K. P. Maruska and A. F. Mensinger, “Acoustic Charac
teristics and Variations in Grunt Vocalizations in the
Oyster Toadfish Opsanus tau,” Environ. Biol. Fishes
84, 325–337 (2009).
163. K. P. Maruska, K. S. Boyle, L. R. Dewan, and
T. C. Tricas, “Sound Production and Spectral Hearing
Sensitivity in the Hawaiian Sergeant Damselfish, Abu
defduf abdominalis,” J. Exp. Biol. 210, 3990–4004
(2007).
164. P. Marvit and J. D. Crawford, “Auditory Discrimina
tion in a SoundProducing Electric Fish (Pollimyrus):
Tone Frequency and ClickRate Difference Detec
tion,” J. Acoust. Soc. Am. 108 (4), 1819–1825 (2000).
165. C. Mazzoldi, M. Scaggiante, E. Ambrosin, and
M. Rasotto, “Mating System and Alternative Tactics
in the Grass Goby (Zosterisessor ophiocephalus),” Mar.
Biol. (Berlin) 137, 1041–1048 (2000).
166. R. D. McCauley and D. H. Cato, “Patterns of Fish
Calling in a Nearshore Environment in the Great Bar
rier Reef,” Philos. Trans. Roy. Soc. Lond. B 355,
1289–1293 (2000).
167. J. R. McKibben and A. H. Bass, “Behavioral Assess
ment of Acoustic Parameters Relevant to Signal Rec
ognition and Preference in a Vocal Fish,” J. Acoust.
Soc. Am. 104 (6), 3520–3533 (1998).
168. J. R. McKibben and A. H. Bass, “Effects of Temporal
Envelope Modulation on Acoustic Signal Recognition
in a Vocal Fish, the Plainfin Midshipman,” J. Acoust.
Soc. Am. 109 (6), 2934–2943 (2001).
169. K. Midling, A. V. Soldal, and J. E. Fosseidengen, and
J. T. “Ovredal, “Calls of the Atlantic Cod: Does Cap
tivity Restrict Their Vocal Repertoire?,” Bioacoustics
12, 233–235 (2002).
170. M. Miyagawa and A. Takemura, “Acoustical Behav
iour of the Scorpaenoid Fish Sebasticus marmoratus,”
Bull. Jpn. Soc. Sci. Fish. 52, 411–415 (1986).
171. P. Moller, Electric Fishes History and Behavior (Chap
man and Hall, London, 1995).
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
1017
172. P. Moller, J. Serrier, P. Belbenoit, and S. Push, “Notes
on the Ethology and Ecology of the Swashi River
Mormyrids (Lake Kainji, Nigeria),” Behav. Ecol.
Sociobiol. 4, 357–368 (1979).
173. J. M. Moulton, “The Acoustical Behaviour of Some
Fishes in the Bimini Area,” Biol. Bull. 114, 357–374
(1958).
174. A. A. Myrberg, Jr., “Ethology of the Bicolor Damself
ish, Eupomacentrus partitus (Pisces: Pomacentridae):
A Comparative Analysis of Laboratory and Field
Behavior,” Anim. Behav. Monogr. 5, 197–283 (1972).
175. A. A. Myrberg, Jr., :”Sensory Mediation of Social
Recognition Processes in Fishes,” in Fish Behaviour
and Its Use in the Capture and Culture of Fishes, Ed. by
J. E. Bardach, J. J. Magnuson, R. C. May, and
J. M. Reinhart (Manila, 1980), pp. 146–178.
176. A. A. Myrberg, Jr., “Sound Communication and
Interception in Fishes,” in Hearing and Sound Com
munication in Fishes, Ed. by A. N. Popper and
R. R. Fay (Springer, Berlin, 1981), pp. 359–426.
177. A. A. Myrberg, Jr., “Sound Production by a Coral Reef
Fish (Pomacentrus partitus): Evidence for a Vocal, Ter
ritorial "KeepOut” Signal,” Bull. Mar. Sci. 60 (3),
1017–1025 (1997).
178. A. A. Myrberg, Jr. and M. Lugli, “Reproductive
Behavior and Acoustical Interactions,” in Communi
cation in Fishes, Ed. by F. ladich, S. P. Collin, P. Mol
ler, and B. G. Kapoor (Sci. Publ., Enfield, 2006).
179. A. A. Myrberg, Jr. and D. R. Nelson, “The Behavior of
Sharks: What Have We Learned?,” Underwater Natur.
20 (1), 92–100 (1990).
180. A. A. Myrberg, Jr. and J. R. Riggio, “Acoustically
Mediated Individual Recognition by a Coral Reef Fish
(Pomacentrus partitus),” Anim. Behav. 33, 411–416
(1985).
181. A. A. Myrberg, Jr. and J. Y. Spires, “Sound Discrimi
nation by the Bicolor Damselfish, Eupomacentrus par
titus,” J. Exp. Biol. 57, 727–735 (1972).
182. A. A. Myrberg, Jr. and J. Y. Spires, “Hearing in Dam
selfishes: An Analysis of Signal Detection Among
Closely Related Species,” J. Comp. Physiol. A 140,
135–144 (1980).
183. A. A. Myrberg, Jr., E. Spanier, and S. J. Ha, “Temporal
Pattering in Acoustic Communication,” in Contrasts in
Behaviour, Ed. by E. S. Reese and F. J. Lighter (John
Wiley and Sons, New York, 1978), pp. 137–179.
184. A. A. Myrberg, Jr., S. J. Ha, and M. J. Shamblott,
“The Sounds of the Bicolor Damselfish (Pomacentrus
partitus): Predictors of Body Size and a Spectral Basis
for Individual Recognition and Assessment,” J.
Acoust. Soc. Am. 94, 3067–3070 (1993).
185. J. M. Nestler, G. R. Ploskey, J. Pickens, et al.,
“Responses of Blueback Herring to HighFrequency
Sound and Implication for Reducing Entrainment at
Hydropower Dams,” N. Am. J. Fish. Manag. 12,
667 – 683 (1992).
186. P. F. Nicoletto and S. H. Linscomb, “Sound Produc
tion by the Sheepshead Minnow, Cyprinodon varie
gates,” Environ. Biol. Fishes 81, 15 – 20 (2008).
187. J. T. Nordeide and E. Kjellsby, “Sound from Spawning
Cod at Their Spawning Grounds,” ICES J. Mar. Sci.
56 (3), 326–332 (1999).
1018 KASUMYAN
188. D. P. Nowacek, “Acoustic Ecology of Foraging Bottle
nose Dolphins (Tursiops truncates), HabitatSpecific
Use of Three Sound Types,” Mar. Mamm. Sci. 21,
587–602 (2005).
189. A. Onuki and H. Somiya, “Two Types of Sounds and
Additional Spinal Nerve Innervation to the Sonic
Muscle in John Dory, Zeus faber (Zeiformes, Teleo
stei),” J. Mar. Biol. Assoc. UK 84, 843–850 (2004).
190. E. Parmentier, P. Vandewalle, and J. P. Lagardére,
“Sound Producing Mechanisms and Recordings in
Three Carapidae Species (Teleostei, Pisces),” J.
Comp. Physiol. A189, 283–292 (2003).
191. E. Parmentier, J. P. Lagardére, P. Vandewalle, and
M. L. Fine, “Geographical Variation in Sound Pro
duction in the Anemonefish Amphiprion akallopisos,”
Proc. Roy. Soc. Lond. B. Biol. Sci. 272, 1697–1703
(2005).
192. E. Parmentier, P. Vandewalle, B. Frederich, and
M. L. Fine, “Sound Production in Two Species of
Damselfishes (Pomacentridae): Plectroglyphididon
lacrymatus and Dascyllus aruanus,” J. Fish. Biol. 69,
491–503 (2006).
193. M. J. Phillips, “The Feeding Sounds of Rainbow
Trout, Salmo gairdneri Richardson,” J. Fish. Biol. 35,
589–592 (1989).
194. C. T. Phillips and C. E. Johnston, “Sound Production
and Associated Behaviours in Cyprinella galactura,”
Environ. Biol. Fishes 82, 265–275 (2008a).
195. C. T. Phillips and C. E. Johnston, “Geographic Varia
tion in Acoustic Signals in Cyprinella galactura,”
Anim. Behav. 75, 617–626 (2008b).
196. C. T. Phillips and C. E. Johnston, “Evolution of
Acoustic Signals in Cyprinella: Degree of Similarity in
Sister Species,” J. Fish. Biol. 74, 120–132 (2009).
197. M. Picciulin, M. Costantini, A. D. Hawkins, and
E. Ferrero, “Sound Emissions of the Mediterranean
Damselfish Chromis chromis (Pomacentridae),” Bioa
coustics 12 (2–3), 236–238 (2002).
198. A. N. Popper, A. Salmon, and A. Parvulescu, “Sound
Localization by the Hawaiian Squirrelfishes, Myripris
tis berndti and M. argyromus,” Anim. Behav. 21, 86–97
(1973).
199. V. R. Protasov, Bioacoustics in Fish (Nauka, Moscow,
1965) [in Russian].
200. V. R. Protasov and M. P. Aronov, “On the Biological
Importance of Sounds of Some Black Sea Fish,”
Biofizika 5 (6), 750–752 (1960).
201. V. R. Protasov and I. D. Nikol’skii, Sounds in the World
of Silence (Pishchevaya Promyshlennost’, Moscow,
1969) [in Russian].
202. V. R. Protasov and E. V. Romanenko, “Sounds Emit
ted by Some Fish and Their Signal Importance,” Zool.
Zh. 41 (10), 1516–1528 (1962).
203. V. R. Protasov, V. I. Tsvetkov, and V. K. Rasshcheperin,
“Acoustic Signaling in Azov Round Goby (Neogobius
melanostomus Pallas),” Zh. Obshch. Biol. 24 (2), 151–
159 (1965).
204. I. Pruzsinszky and F. Ladich, “Sound Production and
Reproductive Behaviour of the Armoured Catfish
Corydoras paleatus (Callichthyidae),” Environ. Biol.
Fishes 53, 183–191 (1998).
JOURNAL OF ICHTHYOLOGY
205. E. Raffinger and F. Ladich, “Acoustic Threat Display
and Agonistic Behaviour in the RedFinned Loach
Yasuhikotakia modesta,” J. Ethol. 27, 239–247 (2009).
206. A. Rakitin, M. M. Ferguson, and E. A. Trippel, “Male
Reproductive Success and Body Size in Atlantic Cod,
Gadus morhua,” Marine Biol. 138, 1977–1985 (2001).
207. J. Ramcharitar, D. P. Gannon, and A. N. Popper,
“Bioacoustics of Fishes of the Family Sciaenidae
(Croakers and Drums),” Trans. Am. Fish. Soc. 135
(5), 1409–1431 (2006).
208. L. RemageHealey, D. P. Nowacek, and A. H. Bass,
“Dophin Foraging Sounds Suppress Calling and Ele
vate Stress Hormone Levels in a Prey Species, the Gulf
Toadfish,” J. Exp. Biol. 209, 4444–4451 (2006).
209. L. Rigley and J. A. Marshall, “Sound Production by
the Loach Botia berdmorei (Pisces, Cobitidae),” Am.
Zool. 11, 632 (1971).
210. J. L. Ripley and P. S. Lobel, “Correlation of Acoustic
and Visual Signals in the Cichlid Fish, Tramitichromis
intermedius,” Environ. Biol. Fishes 71 (4), 389–394
(2004).
211. J. L. Ripley, P. S. Lobel, and H. Y. Yan, “Correlation of
Sound Production with Hearing Sensitivity in the
Lake Malawi Cichlid Tramitichromis intermedius,”
Bioacoustics 12 (2–3), 238–240 (2002).
212. C. M. Roberts and R. F. G. Ormond, “Butterflyfish
Social Behaviour, with Special Reference to the Inci
dence of Territoriality: A Review,” Environ. Biol.
Fishes 34, 79–93 (1992).
213. M. Rocca, M. Trivisonno, M. Picciulin, et al., “Jago
vs. Cassio, Territorial Behaviour in Gobius cruentatus,
Gmelin 1789,” Adv. Ethol., No. 36, 252 (2001).
214. P. H. Rogers and M. Cox, “Underwater Sound as a
Biological Stimulus,” in Sensory Biology of Aquatic
Animals, Ed. by J. Atema, R. R. Fay, A. N. Popper, and
W. N. Tavolga (Springer, New York, 1988), pp. 131–
149.
214. E. V. Romanenko, Physical Bases of Bioacoustics
(Nauka, Moscow, 1974) [in Russian].
215. R. A. Rountree and J. BowersAltman, “Soniferous
Behaviour of the Striped CuskEll Ophidion mar
ginatum,” Bioacoustics 12 (2–3), 240–242 (2002).
216. R. Rountree, P. Perkins, R. D. Kenney, and
K. R. Hinga, “Sounds of Western North Atlantic
Fishes  Data Rescue,” Bioacoustics 12 (2–3), 242–
244 (2002).
217. R. Rountree, C. Goudey, T. Hawkins, et al., “Listen
ing to Fish: Passive Acoustic Applications in Marine
Fisheries,” in Proceedings of the International Work
shop on the Applications of Passive Acoustics to Fisheries,
2002, Ed. by R. Rountree, C. Goudey, T. Hawkins,
J. J. Luczkovich, and D. Mann (Massachusetts Insti
tute of Technology Sea Grant Technical Report)
(Dedham, MA, Cambridge, 2003).
218. R. A. Rountree, R. G. Gilmore, C. A. Goudey, et al.,
“Listening to Fish: Applications of Passive Acoustic to
Fisheries Science,” Fisheries 31 (9), 433–446 (2006).
219. S. Rowe and J. A. Hutchings, “A Link between Soun
Producing Musculature and Mating Success in Atlan
tic Cod,” J. Fish. Biol. 72, 500–511 (2008).
Vol. 49 No. 11 2009
 ACOUSTIC SIGNALING IN FISH
220. M. J. Ryan and E. A. Brenowitz, “The Role of Body
Size, Phylogeny, and Ambient Noise in the Evolution
of Bird Song,” Am. Nat. 126, 87–100 (1985).
221. L. P. Sabaneev, Life and Fishing (Angling) of Our Fresh
water Fish, 3rd ed. (Izdvo A.A. Kartseva, Moscow,
1911) [in Russian].
222. O. Sand, P. S. Enger, H. E. Karlsen, et al., “Avoidance
Responses to Infrasound in Downstream Migrating
European Silver Eels, Anguilla anguilla,” Environ.
Biol. Fishes 57, 327–336 (2000).
223. J. A. Santiago and J. J. Castro, “Acoustic Behaviour of
Abudefduf luridus,” J. Fish. Biol. 51 (5), 952–959
(1997).
224. G. Sará, J. M. Dean, D. D’Amato, et al., “Effect of
Boat Noise on the Behaviour of Bluefin Tuna Thunnus
thynnus in the Mediterranean Sea,” Mar. Ecol. Progr.
Ser. 331, 243–253 (2007).
225. M. H. Saucier and D. N. Baltz, “Spawning Site Selec
tion by Spotted Seatrout, Cynoscion nebulosus, and
Black Drum, Pogonias cromis, in Louisiana,” Environ.
Biol. Fishes 36, 257–272 (1993).
226. H. Schneider, “Physiologische und Morphologische
Untersuchungen zur Bioakustik der Tigerfische
(Pisces, Theraponidae),” Z. Vergl. Physiol. 47, 493–
558 (1964a).
227. H. Schneider, “Bioakustische Untersuchungen an
Anemonenfischen der Gattung Amphiprion (Pisces),”
Z. Morphol. Okol. Tiere 53, 453–474 (1964b).
228. H. Schneider, “Morphology and Physiology of Sound
Producing Mechanisms in Teleost Fishes,” in Marine
BioAcoustics, Ed. by W. N. Tavolga (Pergamon,
Oxford, 1967), Vol. 2, pp. 135–158.
229. A. R. Scholik and H. Y. Yan, “Effects of Underwater
Noise on Auditory Sensitivity of a Cyprinid Fish,”
Hearing Res. 152, 17–24 (2001).
230. K. Scholz and F. Ladich, “Sound Production, Hearing
and Possible Interception Under Ambient Noise Con
ditions in the Topmouth Minnow Pseudorasbora
parva,” J. Fish. Biol. 69, 892–906 (2006).
231. A. Schwarz, “The Inhibition of Aggressive Behaviour
by Sound in the Cichlid Fish, Cichlasoma centrar
chus,” Z. Tierpsychol. 35, 508–517 (1974).
232. E. V. Shishkova, “Registration and Analysis of Fish
Sounds,” Tr. Vses. NauchnoIssled. Inst. Rybn. Khoz.
Okeanogr. 36, 280–294 (1958).
233. E. V. Shishkova, Physical Bases of Localization of Fish
(Pishchepromizdat, Moscow, 1963) [in Russian].
234. J. M. Simöes, P. J. Fonseca, G. F. Turner, and
M. C. P. Amorim, “African Cichlid Pseudotropheus
spp. Males Moan to Females during Foreplay,” J. Fish.
Biol. 72, 2689–2694 (2008).
235. S. D. Simpson, M. Meekan, J. Montgomery, et al.,
“Homeward Sound,” Science 308, 221 (2005).
236. M. E. Smith, A. S. Kane, and A. N. Popper, “Noise
Induced Stress Response and Hearing Loss in Gold
fish (Carassius auratus),” J. Exp. Biol. 207, 427–435
(2004).
237. V. V. Sorokin and D. S. Simakov, “Use of Acoustic Sig
nals in Fishing Heatfish,” in Biodiversity of the Upper
Volga Region: Modern State and Problems of Preserva
tion, Materials of Regional Scientific and Practical Con
JOURNAL OF ICHTHYOLOGY Vol. 49 No. 11 2009
1019
ference Dedicated to the Memory of A.S. Petrovskii
(Yaroslavl, 2004), pp. 137–138.
237. E. Spanier, “Aspects of Species Recognition by Sound
in Four Species of Damselfishes, Genus Eupomacen
trus (Pisces: Pomacentridae),” Z. Tierpsychol. 51,
301–316 (1979).
238. M. W. Sprague and J. J. Luczkovich, “Do Striped
CuskElls Ophidion marginatum (Ophidiidae) Produce
the “Chatter” Sound Attributed to Weakfish Cynoscion
regalis (Sciaenidae)?,” Copeia, No. 3, 854–859
(2001).
239. M. W. Sprague and J. J. Luczkovich, “Measurement of
an Individual Silver Perch Bairdiella chrysoura Sound
Pressure Level in a Field Recording,” J. Acoust. Soc.
Am. 116, 3186–3191 (2004).
240. J. C. Steinberg, W. C. Cummings, B. D. Brahy, and
J. Y. MacBain, “Further BioAcoustic Studies Off the
West Coast of North Bimini, Bahamas,” Bull. Mar.
Sci. 15, 942–963 (1965).
241. M. Stepanek, “Beiträge zur Bioakustik der Bin
nengewässer. II. Fressgeräusche von Karpfen und
Elritzen,” Archiv Hydrobiol. 33, 423–430 (1968).
242. M. Takayama, A. Onuki, T. Yosino, et al., “Sound
Characteristics and the Sound Producing System in
Silver Sweeper, Pempheris schwenkii (Perciformes:
Pempheridae),” J. Mar. Ass. U.K 83, 1317–1320
(2003).
243. A. Takemura, T. Takita, and K. Mizue, “Studies on the
Underwater Sound—VII. Underwater Calls of the
Japanese Marine Drum Fishes (Sciaenidae),” Bull.
Jpn. Soc. Sci. Fish. 44, 121–125 (1978).
244. W. N. Tavolga, “Visual, Chemical and Sound Stimuli
in SexDiscriminatory Behavior of the Gobiid Fish
Bathygobius soporator,” Zoologica 41, 49–64 (1956).
245. W. N. Tavolga, “Underwater Sounds Produced by Two
Species of Toadfish Opsanus tau and Opsanus beta,”
Bull. Mar. Sci. 8, 278–284 (1958a).
246. W. N. Tavolga, “Underwater Sounds Produced by
Males of the Blenniid Fish, Chasmodes bosquianus,”
Ecology 39, 759–760 (1958b).
247. W. N. Tavolga, “Sonic Characteristics and Mecha
nisms in Marine Fishes,” in Marine BioAcoustics, Ed.
by W. N. Tavolga (Pergamon, New York, 1964), Vol. 1,
pp. 195–211.
248. W. N. Tavolga, “Sound Production and Detection,” in
Fish Physiology, Ed. by W. S. Hoar and D. J. Randall
(Academic, New York, 1971), Vol. 5, pp. 135–205.
249. W. Templeman and V. M. Hodder, “Variation in Fish
Length, Sex, Stage of Sexual Maturity, and Season in
the Appearance and Volume of the Drumming Muscle
of the SwimBladder in the Haddock, Melamogram
mus eaglepinus,” J. Fish. Res. Board Can. 15, 355–390
(1958).
250. R. F. Thorson and L. F. Fine, “Crepuscular Changes in
Emission Rate and Parameters of the Boatwhistle
Advertisement Call of the Gulf Toadfish, Opsanus
beta,” Environ. Biol. Fishes 63, 321–331 (2002a).
251. R. F. Thorson and L. F. Fine, “Acoustic Competition
in the Gulf Toadfish, Opsanus beta: Acoustic Tagging,”
J. Acoust. Soc. Am. 111 (5), 2302–2307 (2002b).
1020 KASUMYAN
252. N. Tolimieri, O. Haine, A. Jeffs, et al., “Directional
Orientation of Pomaventrid Larvae to Ambient Reef
Sound,” Coral Reefs 23, 184–191 (2000a).
253. N. Tolimieri, A. Jeffs, and J. C. Montgomery, “Ambi
ent Sound as a Cue for Navigation by the Pelagic Lar
vae of Reef Fishes,” Mar. Ecol.: Proc. Ser. 207, 219–
224 (2000b).
254. K. L. Tolstoganova, “Acoustic Activity in Beluga Huso
huso,” Technical Compendium, Proc. 4th Int. Symp.
on Sturgeon” (2001), p. 036.
255. P. Torricelli and R. Romani, “Sound Production in the
Italian Freshwater Goby, Padogobius martensi,”
Copeia, No. 1, 213–216 (1986).
256. P. Torricelli, S. Malavasi, N. Novarini, et al., “Elonga
tion of Fin Rays in Parental Males of Zosterisessor
pphiocephalus,” Environ. Biol. Fishes 58, 105–108
(2000).
257. R. Tower, “The Production of Sound in the Drum
Fishes, the Searobin and the Toadfish,” Ann. N. Y.
Acad. Sci. 18, 149–180 (1908).
257. T. C. Tricas, S. M. Kajiura, and R. K. Kosaki, “Acous
tic Communication in Territorial Butterflyfish: Test of
the Sound Production Hypothesis,” J. Exp. Biol. 209,
4994–5004 (2006).
258. G. F. Turner, “Explosive Speciation of African Cichlid
Fishes,” in Evolution of Biological Diversity, Ed. by
A. E. Magurran and R. M. May (Oxford Univ.,
Oxford, 1999), pp. 217–299.
259. W. Valinski and L. Rigley, “Function of Sound Produc
tion in the Skunk Loach Botia horae (Pisces, Cobiti
dae),” Z. Tierpsychol. 55 (2), 161–172 (1981).
260. L. Vasantha, A. Jeyakumar, and M. A. Pitchai, “Influ
ence of Music on the Growth of Koi Carp, Cyprinus
carpio (Pisces: Cyprinidae),” Naga 26 (4), 25–26
(2003).
261. R. O. Vasconcelos and F. Ladich, “Development of
Vocalization, Auditory Sensitivity and Acoustic Com
munication in the Lusitnian Toadfish Halobatrachus
didactylus,” J. Exp. Biol. 211, 502–509 (2008).
262. R. O. Vasconcelos, M. C. P. Amorim, and F. Ladich,
“Effects of Ship Noise on the Detectability of Com
munication Signals in the Luisitanian Toadfish,” J.
Exp. Biol. 210, 2104–2112 (2007).
263. H. I. Vester, L. P. Folkow, and A. S. Blix, “Click Sound
Produced by Cod (Gadus morhua),” J. Acoust. Soc.
Am. 115 (2), 914–919 (2004).
264. M. Wahlberg and H. Westerberg, “Sounds Produced
by Herring (Clupea harengus) Bubble Release,” Aquat.
Living Resources 16, 271–275 (2003).
265. P. M. Waser and M. S. Waser, “Experimental Studies of
Primate Vocalization: Specializations for Long Dis
tance Propagation,” Z. Tierpsychol. 43, 239–263
(1977).
266. J. F. Webb, “Laterophysic Connection: A Unique Link
Between the Swimbladder and the Lateral Line System
in Chaetodon (Perciformes: Chaetodontidae),” Copeia,
No. 4, 1032 (1998).
267. J. F. Webb and W. L. Smith, “The Laterophysic Con
nection in Chaetodontid Butterflyfish: Morphological
JOURNAL OF ICHTHYOLOGY
Variation and Speculations on Sensory Function,”
Philos. Trans. Roy. Soc. Lond. B 355, 1125–1129
(2000).
268. J. F. Webb, W. L. Smith, and D. R. Ketten, “The Lat
erophysic Connection and Swim Bladder of Butterfly
fishes in the Genus Chaetodon (Perciformes: Chaet
odontidae),” J. Morphol. 267, 1338–1355 (2000).
269. A. Whang and J. Janssen, “Sound Production
Through the Substrate During Reproduction in the
Mottled Sculpin, Cottus bairdi (Cottidae),” Environ.
Biol. Fishes 40 (2), 141–148 (1994).
270. B. Wilson, R. S. Batty, and L. M. Dill, “Pacific and
Atlantic Herring Produce Burst Pulse Sounds,” Proc.
Roy. Soc. London, Ser. B, Biol. Sci. 271, S95–S97
(2004).
271. H. E. Winn, “Vocal Facilitation and the Biological Sig
nificance of Toadfish Sounds,” in Marine BioAcous
tics, Ed. by W. N. Tavolga (Pergamon, New York,
1964), Vol. 2, pp. 213–231.
272. H. E. Winn, “Acoustic Discrimination by the Toadfish
with Comments on Signal Systems,” in Behavior of
Marine Animals: Current Perspectives in Research.
Vol. 2: Vertebrates, Ed. by H. E. Winn and B. L. Olla
(Pergamon Press, New York, 1972), pp. 361–385.
273. H. E. Winn, J. A. Marshall, and B. Hazlett, “Behavior,
Diel Activities and Stimuli That Elicit Sound Produc
tion and Reactions to Sounds in the Longspine Squir
relfish,” Copeia, No. 2, 413–425 (1964).
274. B. D. Wisenden, J. Pogatshnik, D. Gibson, et al.,
“Sound the Alarm: Learned Association of Predation
Risk with Novel Auditory Stimuli by Fathead Min
nows (Pimephales promelas) and Glowlight Tetras
(Hemigrammus eruthrozonus) after Single Simulta
neous Pairing with Conspecific Chemical Alarm
Cues,” Environ. Biol. Fishes 81 (2), 141–147 (2008).
275. K. J. Wright, D. M. Higgs, A. J. Belanger, and
J. M. Leis, “Auditory and Olfactory Abilities of Pre
Settlement Larvae and PostSettlement Juveniles of a
Coral Reef Damselfish (Pisces: Pomacentridae),”
Mar. Biol. (Berlin) 147, 1425–1434 (2005).
276. L. E. Wysocki and F. Ladich, “The Ontogenetic
Development of Auditory Sensitivity, Vocalization and
Acoustic Communication in the Labyrinth Fish Tri
chopsis vittata,” J. Comp. Physiol. A 187, 177–187
(2001).
277. L. E. Wysocki and F. Ladich, “The Representation of
Conspecifics Sound in the Auditory Brainstem of
Teleost Fishes,” J. Exp. Biol. 206, 2229–2240 (2003).
278. L. E. Wysocki, J. P. Dittami, and F. Ladich, “Ship
Noise and Cortisol Secretion in European Freshwater
Fishes,” Biol. Conserv. 128, 501–508 (2006).
279. R. Zelick, D. Mann, and A. N. Popper, “Acoustic
Communication in Fishes and Frogs,” in Comparative
Hearing: Fish and Amphibians, Ed. by R.R. Fay and
A.N. Popper (Springer, New York, 1999), pp. 363–
411.
280. N. Zograf, “Music of Nature (NaturalHistorical
Essays). The Second Essay. Music of Water Inhabit
ants,” Russk. Obozrenie 3, 765–781 (1890).
Vol. 49 No. 11 2009