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J. exp. Biol. (1982), 96, 367-376
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AUDITORY ACUITY IN THE SEA CATFISH
(ARJUS FELIS)
BY WILLIAM N. TAVOLGA
Mote Marine Laboratory, Sarasota, Florida
(Received 15 April 1981)
SUMMARY
Frequency discrimination limens and signal-to-noise ratios were determined for the sea catfish, Arius felts, using avoidance-conditioning techniques. The lowest frequency discrimination limens had values of about
2-5 % at 100 Hz. Other determinations were 3-5 % at 200 Hz, and 5 % at
400 Hz, but these values were significantly greater if the test frequencies
were higher than the reference. Signal-to-noise ratios were 14 dB at 100 Hz,
18 dB at 200 Hz, and 24 dB at 400 Hz, with reference to the spectrum level
of broad-band noise. These findings, and previous measurements of acuity,
are discussed in relation to echolocation in Arius, which is known to involve
sounds in the 100-200 Hz range.
INTRODUCTION
The estuarine sea catfish, Arius felis, produces sounds that consist primarily of
short bursts of low-frequency pulses with a dominant frequency of about 100 Hz
(Tavolga, 1962; Breder, 1968). Reflexions and reverberations of these sounds from
nearby objects have been found to interact with the outgoing sound bursts and produce changes in the relative intensities of harmonics, even in the low frequency range
(Tavolga, 1971a). These sounds have been shown to be used in a primitive form of
echolocation (Tavolga, 1976). Both lateral line and inner ear pathways may be used,
and directional characteristics of the swim bladder could enhance the echolocating
function (Tavolga, 1977).
As a first stage in the investigation of audition in Arius, Popper & Tavolga (1981)
have provided a basic audiogram for the species correlated with the morphology of
the inner ear. The present study is directed at the question of the auditory capacities
that could be related to the acoustical obstacle detection behaviour: specifically, the
frequency and signal-to-noise discrimination limens.
METHODS OF TRAINING AND TESTING
The animals used in this study were juveniles of the sea catfish, Arius felis, collected
from the buccal cavities of males (see Merriman, 1940, for life-history details). They
were maintained in aquaria for about 20 days until they attained a size of 4-5—5 cm in
368
W. N. TAVOLGA
total length. Initially, about ioo individuals were started in the avoidance training
procedures. Based upon their readiness to acquire the avoidance response, eventually
ten animals were selected for the frequency discrimination tests and ten were used in
the masking noise tests. The animals selected for testing were kept in individual 75 1
(2 gallon) aquaria supplied with running sea water.
The technique of obtaining auditory thresholds by means of avoidance conditioning
has been described in detail elsewhere (Tavolga & Wodinsky, 1965; Tavolga, 1966,
1967; Jacobs & Tavolga, 1967, 1968; Popper, 1970). In brief, the subject was trained
and tested in a shuttle-box, in which it had to learn to swim across a barrier to escape
or avoid an electric shock after the onset of an acoustic signal. Intertrial barrier
crossings (false positive responses) were kept at a low negligible level by control of
the water depth over the barrier. A crossing rate of not more than 6/min of intertrial
time was considered adequate, i.e. the probability of a false positive response is
extremely low. Crossing rates, however, were quite variable, and occasional spurts of
activity were not uncommon.
The training and testing was done in a sound-proof chamber, with a 30 cm (12 in)
loudspeaker mounted in the ceiling, as described by Jacobs & Tavolga (1967) and
Popper (1970). The chamber was air-tight so that the stimulus applied was virtually
a pure pressure wave (Parvulescu, 1964, 1967). Signal intensity was calibrated by a
hydrophone in the test tank, and an air microphone set just above the central barrier
of the test tank. The audio attenuator was calibrated to an accuracy of better than
o-1 dB; the variation in the test tank was within 2 dB at different points in the tank.
The ambient noise level, measured in the 20-1500 Hz band, had total pressure of
about — 55 dB re 1 /tbar (abbreviated here as dB/ibar); the spectrum level in this band
was calculated to be about — 85 dB/ibar/Hz, i.e. significantly below threshold at any
test point (Popper & Tavolga, 1981), thus eliminating the possible masking effect of
ambient noise.
For training, electric shocks were delivered through a pair of stainless-steel screen
electrodes, as previously described (Popper & Tavolga, 1981). The audio signals were
single frequency sine waves, checked for quality on an oscilloscope, and calibrated to
an accuracy of at least 1 % with a digital frequency counter. These signals were turned
on and off by an optoelectric switch with a rise time of about 20 ms to avoid possible
switching transients. All timing and control was done by a computer (Heath H-8)
with an external TTL and relay interface. Responses were timed by the internal clock
of the computer, which also determined, controlled and recorded the sound levels.
The data were stored on discs for later printout and analysis.
Frequency discrimination measurements used the method of alternate pulsed tones,
first described for fishes by Dijkgraaf & Verheijen (1950), and subsequently employed
by Jacobs & Tavolga (1968). Each subject was initially exposed in the test chamber to
several minutes of the reference frequency, with a pulse cycle of 100 ms on and 50 ms
off. The conditioned stimulus was an alternation of the reference and test frequency.
All the subjects were first trained with a reference frequency of 100 Hz and a test
frequency of 150 Hz, and a criterion of 90 % avoidances was attained in 3-5 days.
Each subject was tested daily at a different test frequency that was randomly selected,
but eventually every animal was tested 5 times at each test frequency. A test session
Auditory acuity in the sea catfish
369
consisted of 50 trials. When changed to a new reference frequency, 3 days of retraining was found necessary, and it was apparent that these animals were poorly able
to generalize from one reference frequency to another.
Threshold determinations in the presence of masking noise were done with the
staircase method, starting with a signal level substantially above threshold and above
masker level. The method was as described for obtaining masked thresholds in other
fish species (Tavolga, 1974), and similar to that used for obtaining absolute thresholds
(Popper & Tavolga, 1981). The trial timing was as above; the staircase steps were in
1 dB increments; each threshold determination was based on at least 20 changes from
avoidance to escape or vice versa; each of 10 subjects was tested 10 times for each of
the signal-to-noise conditions. The masker was produced by a Gaussian random-noise
generator whose output was modified by an active band-pass filter with skirt characteristics of 24 dB drop/octave on either side of the 3 dB down points. The masking
bandwidth was determined on the basis of preliminary observations to be identical in
effect to broad-band noise. The bandwidths selected were certainly broader than the
theoretical critical band (assuming critical band function as in mammalian hearing),
and the frequency discrimination limens would indicate that critical bands, if existing
in this species, must be much narrower than the bandwidths used as maskers. Masking
band shape and relative signal levels were observed and recorded by means of a
spectrum analyser (EMR Model 1510). The bandwidth of the masker is given as being
between the 3 dB down points, and the spectrum level of the noise (in dB/ibar/Hz)
was calculated from hydrophone and microphone measurements as measured level
(in dB/^bar) minus 10 times the log of the bandwidth. The single frequency signal
was set to the logarithmic centre of the masking band, and the initial signal level was
at - 10 dB/ibar for the 100 and 200 Hz signals ,and o dB/m for the 400 Hz signal.
These starting levels were about 10 dB above the masker level, 30 dB above the spectrum noise level, and 40 dB above absolute threshold (based on data from Popper &
Tavolga, 1981).
RESULTS
Under the same acoustical test conditions, the variations among individuals and
among replications for each individual were not significant so the results are presented
as pooled data.
Acoustic amplitude values are given here as 'dB/ibar', i.e. dB re 1 /ibar. These
figures can be converted into values re 1 Pa by subtracting 20 dB (1 Pascal = 1 0 dyn/
cm 2 = 10/ibars).
Frequency discrimination
The results of the tests are given in terms of the percentage of avoidance in a series
of 50 trials (Table 1). Ten subjects were tested 5 times under each stimulus condition,
so that every percentage value represents a mean of 50 replications. The frequency
difference is given in terms of Hz and in terms of percentage difference from the
reference. The method of stimulus presentation was essentially that of 'constant
stimuli differences' as defined by Guilford (1954), and a psychometric function curve
was generated. The difference limen, defined as the stimulus frequency difference at
37°
W. N. TAVOLGA
Table i. Summary of frequency discrimination data in Arius felis
Frequency (Hz)
Difference
•»
iiiiien
Reference
Test
IOO
150
SO
120
20
no
10
108
106
105
104
103
200
8
6
S
4
3
102
2
IOI
1
1
99
98
97
96
95
94
3
4
5
6
92
90
10
240
20
220
10
210
208
206
S
4
3
202
t
198
196
2
194
192
400
(%)
2
8
1
3
190
4
5
180
160
20
10
480
460
20
44°
10
420
5
410
3
39O
380
360
3
5
IS
10
34°
15
320
20
Avoidances +/— <r
(% of trials)
947 + / - 3'4
92-4+/-2-4
9I-7+/-3-o
85-1 + / - 2-8
8i-7+/-3-3
77-4+/-47
72-3 + / - 57
56-0 + / - 7-1
46-3 +/-a-9
27-2+/-4-8
22-5 + / - 3-2
466+/-3-7
53-6+/-63
74-7+/-2-8
857+/-3-5
86-8 + / - S-2
928+/-37
949+/-29
95-0 + / - 3-3
8I-8+/-3-8
56-3 + / - 9 - 8
47-9+/-3-5
17-3 +/-3-6
12-5 + / - 3-i
i9'S + / - 59
297 +/-TO
457+/-8-4
56-1 + / - 7 - 3
75-0 + / - 7-4
97-9 + / - 17
96-8 + / - 19
854+/-59
644+/-38
408 +/— 10-4
19-3 + / - 6-2
12-9 +/— a-i
IJ-9 + / - 3-6
511 + / - 73
8o-7+/-4-i
89-6 + / - 3-2
87-2+/-4-0
which there is a 50 % probability of a correct response, can be estimated by linear
interpolation.
With the ico Hz reference frequency, the difference limen lay between 2 and 3 %
(between 2 and 3 Hz), and there was no significant difference between the conditions
where the test frequency was above or below the reference.
At the 200 Hz reference frequency, there was a small but significant difference
between the conditions where the test frequency was above or below the reference.
The 50% difference limen occurred between 4 and 5 % (8 and 10 Hz) when the test
frequency was higher, but this limen was between 3 and 4 % (6 and 8 Hz) when the
test freauencv was below the reference.
Auditory acuity in the sea catfish
371
Table 2. Summary of signal/noise ratio data for Arius felis
Masking noise
Total level (dB/ibar)
Spectrum level (dB/tbar)
Bandwidth (Hz)
Signal frequency (Hi)
MeanS/N + / - (r(dB)
— 20
-42
I2O-29O
— 20
-39
75-I5O
—10
-36
200-600
100
2OO
400
14-1 + / - 23
17-9 + / — i-6
24-a + / - 2-s
This distinction was even more apparent at the 400 Hz reference. The 50 % limen
lay between 10 and 15 % (40 and 60 Hz) with the test frequency higher, and close to
5 % (20 Hz) when the frequency was lower.
Signal-to-noise ratios
Ten subjects were exposed to each of the three signal and masker conditions, and
each was tested for threshold 10 times under the three conditions. Signal-to-noise
ratio (Table 2) was determined as the difference between the spectrum level of the
masker (in dB/ibar/Hz) and the threshold level (in dB/^bar). Each of the signal-tonoise values is a mean of the results for each subject, i.e. a mean of means, but this
does not differ significantly from a value calculated as a mean of 100 independent
determinations. The mean of means method gives a slightly higher standard deviation
value.
A comparison of the signal-to-noise values at 100 Hz and at 200 Hz shows a
significant difference: t = 4-3 and P <^ o-ooi. When compared to values obtained
with the signal at 400 Hz the differences are obviously significant.
DISCUSSION AND CONCLUSIONS
The hearing of Arius appears to be most acute in the 100-200 Hz range. The highest
absolute sensitivity is in this range (Popper & Tavolga, 1981), as shown in Fig. 1. The
present data show that frequency discrimination and signal-to-noise ratios are best
around these frequencies.
The frequency discrimination limens of Arius are compared with the other available
data for Ostariophysi (fish with Weberian apparatus) in Table 3. The two reports on
the goldfish yielded virtually identical results, although the techniques were quite
different. These data are probably not significantly different from the values for
Phoxinus. At 200 Hz the discrimination limen for Arius is well within the scope of the
goldfish data at that frequency, but the limen at 100 Hz is about 2-5 %, as compared
to the 5 % figure for the goldfish (Fay, 1970). The Arius data are even more distinctly
different at 400 Hz. The lowest limen is at 5 %, as compared to 3-5 % for the goldfish.
However, the limen taken when the test frequency was above the reference was about
I
3 %• This value is more in line with the limens for non-ostariophysans, which range
above 15 % and may be as high as 50% (see reviews by Tavolga, 1971 b; Fay, 1974a;
Fay & Popper, 1980; Hawkins, 1981). Noting that the audiogram in Arius rises steeply
above 400 Hz, it may be that frequency discrimination as such no longer operates,
and the discrimination between the two signals may be done on an amplitude or some
basis. A similar condition may explain some of the results at 200 Hz.
372
W. N. TAVOLGA
Ictaluna
10
j
Carasslus
0
I
-10
* -20
e
5 -30
-40
-50
50
100
200
400 600 1000
Frequency (Hz)
2000
5000
Fig. i. Auditory thresholds in the sea catfish, Arius felts, compared with the goldfish, Carassiw
aurotta, and the bullhead catfish, Ictahrrus nebtdosut. (From Popper & Tavolga, 1981.)
Table 3. Frequency discrimination limens in teleost fishes
(Limens in % at test frequency in Hz.)
Species
o/
/o
Hz
Reference
Minnow (Phoximu)
Goldfish (Carastiut)
30
400-800
Dijkgraaf & Verheijen (1950)
Jacobs & Tavolga (1968)
Jacobs & Tavolga (1968)
Jacobs & Tavolga (1968)
Fay (1970)
Fay (1970)
Fay (1970)
Fay (1970)
Fay (1970)
Fay (1970)
Fay (1970)
Present data
Present data
Present data
Present data
Present data
200
3'4
SO
80
5O
3-5
3'5
43
4-3
46
Catfish (Arius)
500
IOOO
50
IOO
3OO
400
600
800
IOOO
IOO
35
45
SO
130
200-down
300-up
400-down
400-up
It is now evident that at least some teleost species are capable of frequency discrimination, but the mechanism by which this is accomplished is still a topic of some
controversy. In mammals and other terrestrial vertebrates, there is a cochlea with a
long basilar membrane, and this is the structure which makes frequency discrimination possible through the operation of the well-known place principle (von B^kesy,
1960J. In essence, he proposed that since there is a distribution of frequencies over
the surface of the basilar membrane, such regional differences in sensitivity must
account for frequency discrimination. Teleost fishes, however, can make frequency
discriminations in spite of their lack of a cochlea as such.
Auditory acuity in the sea catfish
373
One hypothesis for a frequency analysis mechanism in fishes has been the so-called
'bongo-drum' theory presented by van Bergeijk (1967). He proposed that the otolithmacula complex can behave like a bounded membrane with sufficient asymmetry to
resonate at different loci at different input frequencies. The alternative model, preferred by Wever (1969) and Fay (1970, 1974 b), is the volley principle, and this
essentially moves the frequency discrimination mechanism into the central nervous
system. Fay (1981) has noted that the goldfish auditory system is evidently capable of
preserving the temporal structure of complex sounds with great precision, and this
could account for frequency analysis in the time domain rather than through spectral
processing.
The frequency range of hearing in fishes is much narrower than in mammals, and
where there is evidence for frequency analysis capability, the analysis is much coarser.
Therefore either the place principle or the volley principle would be plausible
hypotheses. The only experimental data that bear directly on this question are those
of Enger (1981), who exposed the sculpin, Coitus scorpius, to high intensity sound at
different frequencies. Behavioural evidence showed the deterioration of hearing in the
range corresponding to that of the high-intensity stimulus, and particular loci or areas
of the macula exhibited physical damage. For the first time, the existence of a place
principle in the ear of a fish could be demonstrated.
The different explanations of frequency analysis in the fish ear need not be considered mutually exclusive. There is no reason to assume that a volley system must
operate without a place principle, and perhaps we should look for ways in which these
two mechanisms could interact, possibly synergistically.
Indirect evidence for a place principle is derived from the notion of a critical band,
defined originally by Fletcher (1940) as the narrowest band of noise to produce the
maximum amount of masking of a signal. Direct measurement of a critical band is
complex and tedious, since it involves variation of the noise bandwidth and a determination of masked threshold for each different noise band. If one measures the
threshold to a single frequency signal in the presence of a broad band of masking
noise, a value, in dB re the noise level, is generated. This signal-to-noise ratio has
been termed the 'critical ratio' (Hawkins & Stevens, 1950), and is arithmetically
convertible to the critical band width by the equation :
critical band in Hz = antilog (critical ratio/10).
Scharf (1961, 1970) recommended an empirically derived correction adding 4 dB to
the critical ratio value, but the basic idea that a signal-to-noise ratio by itself can be
used to determine a critical band still remains. This idea holds for mammals and
possibly other terrestrial vertebrates, but the notion is rooted in the acceptance of the
place principle for frequency analysis. In fishes, the place principle is still a hypothesis
to be tested and, consequently, the signal-to-noise ratio cannot be used as a measure
of critical band without appropriate cautions. This indirect approach to the study of
frequency analysis in fishes has been used for a few different species, and the results
are summarized in Table 4.
In most species tested, the signal-to-noise ratio is about 20 dB, but in two cases it
is significantly lower: the squirrelfish, Holocentrus, and the sea catfish, Anus. The
18 dB value is equivalent to that reported for human hearing at 1000 Hz (Hawkins &
374
W. N . TAVOLGA
Table 4. Signal/noise ratios in several teleost species
Species
Goldfish (Carassius)
Pinfish (Lagodon)
Grunt (Haemulcn)
Mouth-breeder (Tilapia)
Squirrelfish (Holocentrui)
Cod (Gadus)
Bonefuh (Albulo)
Sea catfish (Ariut)
S/N
S/NO(dB)
Frequency (Hz)
22
20
5°°
30
500
20
24
200
500
23
300
14
20
500
800
20
100
22
S°o
14
100
18
200
24
400
Reference
Tavolga (1974)
Fay (1974)
Tavolga (1974)
Tavolga (1967)
Tavolga (1967)
Tavolga (1974)
Tavolga (1967)
Tavolga (1967)
Buerkle (1968)
Tavolga (1974)
Present data
Present data
Present data
Stevens, 1950), and the 14 dB value seems to show that the hearing acuity in these two
species is actually better than that of the human. If the signal-to-noise ratio, i.e. the
critical ratio, were indeed related to the frequency discrimination limen, then the
squirrelfish and the sea catfish should show a better frequency discriminatory ability
than the goldfish. The present data for Arius at 100 Hz show a limen of 2-5 % while
the goldfish is significantly higher, i.e. 5 %. At 200 Hz, however, the signal-to-noise
ratios of the two species are within 2 dB and their frequency discrimination limens
are probably not significantly different. Indirectly, therefore, there is additional
support for the operation of a place principle in the fish ear.
Unlike the system in echolocating specialists such as dolphins and most bats,
echolocation in Arius involves low-frequency sounds whose duration is such as to
allow the mixing of outgoing signals and incoming echoes (Tavolga, 1971a). This is
actually akin to the natural echolocating abilities in humans, and involves the alteration
of the perceived sound complex, termed a change in the 'sound color' by Wilson
(1967). The capacity of an organism to utilize this sort of information must depend
on a high sensitivity in the low-frequency range, an efficient signal-to-noise separation,
and the smallest possible frequency discrimination limen. It is evident that Arius has
an unusually high sensitivity in the 100-200 Hz range (Popper & Tavolga, 1981), and
data presented here show that in this range signal-to-noise and frequency discrimination capacities are also excellent.
The recent volume on animal sonar systems edited by Busnel & Fish (1980), contains several models of echolocation systems, but these appear to be appropriate only
for dolphins, bats, and a few additional species of mammals and some birds. The use
of a Doppler shift, for example, as presented by Altes (1980), is unlikely to occur in
fishes since their frequency discrimination would not be adequate for such a task at
low frequencies. Spectral analysis, however, appears to be quite within the capacities
of fishes, and should make it possible to perceive the interference patterns produced
by the interaction of the outgoing and returning signals (Johnson, 1980). The total
effect for the fish may actually be akin to the sonic holograph as conceived by Greguss
Auditory acuity in the sea catfish
375
(1980). One important piece of information about Arius that could bear on this
problem would be the extent to which this species can detect phase changes. It is
probable that the extremes of compression v. rarefaction should be detectable, as
shown for the goldfish by Piddington (1972).
It would be interesting to determine if other teleost species have similar echolocating
abilities, and, indeed, it would be surprising if Arius felts were unique in this field.
Other ariids, such as the gaff-top-sail catfish Bagre marinus, are known as sound
producers (Tavolga, 1962), and there may be many unrelated species to fit the model.
One group that deserves attention would be the squirrelfishes (Holocentridae), whose
sonic output (Winn, Marshall & Hazlett, 1964; Horch & Salmon, 1973) and auditory
function (Coombs & Popper, 1979; Tavolga, 1967, 1974; Tavolga & Wodinsky, 1963)
possess the requirements for acoustic obstacle detection as exemplified by Arius.
This work was supported by grant no. NS-13746 from the National Institute of
Neurological and Communicative Disorders and Stroke. Dr Arthur N. Popper was
extremely helpful through his comments and suggestions on the study and the
manuscript.
REFERENCES
ALTES, R. A. (1980). Models for echolocation. In Animal Sonar Systems (ed. R.-G. Busnel and J. F.
Fish), pp. 625-671. New York: Plenum Press.
BRHDER, C. M., JR (1968). Seasonal and diurnal occurrences of fish sounds in a small Florida bay .Bid.
Am. Mus. Nat. Hist. 138, 325-378.
BUERKLE, U. (1968). Relation of pure tone thresholds to background noise level in the Atlantic cod
(Gadus morhua). J. Fish. Ret. Bd Canada 36, 1113-1119.
BUSNEL, R.-G. & FISH, J. F. (1980). Animal Scnar Systems. New York: Plenum.
COOMBS, S. & POPPER, A. N. (1979). Hearing differences among Hawaiian squirrelfihs (family Holocentridae) related to differences in the peripheral auditory system. J. comp. Pkysiol. 13a, 203-207.
DIJKORAAF, S. & VERHEITEN, F. J. (1950). Neue Versuche liber das Tonunterscheidungsvermfigen der
Elritze. Z. vergl. Pkysiol. 3a, 248-256.
ENCER, P. S. (1981). Frequency discrimination in teleosts - central 01 peripheral? In Hearing and Sound
Communication in Fishes (ed. W. N. Tavolga, A. N. Popper and R. R. Fay). New York: SpringerVerlag. (In the Press.)
FAY, R. R. (1970). Auditory frequency discrimination in the goldfish (Carassius auratus). J. ccmp.
Physiol. Psychol. 73, 175-180
FAY, R. R. (1974a). Auditory frequency discrimination in vertebrates. J. Acoust. Soc. Am. 56, 206-209.
FAY, R. R. (19746). Masking of tones by noise for the goldfish {Carassius auratus). J. comp. Physiol.
Psychol. 84, 708-716.
FAY, R. R. (1981). Discharge patterns and the coding of acoustic information in the eighth nerve. In
Hearing and Sound Communication in Fishes (ed. W. N. Tavolga, A. N. Popper and R. R. Fay). New
York: Springer-Verlag. (In the Press.)
FAY, R. R. & POPPER, A. N. (1979). Structure and function in teleost auditory systems. In Comparative
Studies of Hearing in Vertebrates (ed. A. N. Popper and R. R. Ray), pp. 3-42. New York: SpringerVerlag.
FLETCHER, H. (1940). Auditoiy patterns. Rev. Mod. Phys. ia, 47-65.
GREGUSS, P. (1980). Models of spatial information processing in biosonar systems and methods suggested to validate them. In Animal Sonar Systems (ed. R.-G. Busnel and J. F. Fish), pp. 731-745.
New York: Plenum.
GUILFORD, J. P. (1954). Psychometric Methods. New York: McGraw-Hill.
HAWKINS, A. D. (1981). The hearing abilities of fish. In Hearing and Sound Comrmmicatien in Fishes
(ed. W. N. Tavolga, A. N. Popper and R. R. Fay). New York: Springer-Verlag. (In the Press.)
HAWKINS, J. E. & STEVENS, S. S. (1950). The masking of pure tones and of speech by white noise.
J. Accust. Soc. Am. aa, 6-13.
HORCH, K. & SALMON, M. (1973). Adaptations to the acoustic environment by the squirrelfishes
Myripristis violaceus and M. pralinius. Mar. Behav. Physiol. a, 121-139.
376
W. N. TAVOLGA
JACOBS, D. W. & TAVOLGA, W. N. (1967). Acoustic intensity limens in the goldfish. Anim. Behav. 15,
3*4-335JACOBS, D. W. & TAVOLGA, W. N. (1968). Acoustic frequency discrimination in the goldfish. Anim.
Behav. 16, 67-71.
JOHNSON, R. A. (1980). Energy spectrum analysis in echolocation. In Animal Sonar Systems (ed. R.-G.
Busnel and J. F. Fish), pp. 673-693. New York: Plenum.
MERRIMAN, D. (1940). Morphological and embryological studies on two species of marine catfish,
Bagre marinus and Galeichthys felis. Ztologica 35, 221-248.
PARVULESCU, A. (1964). Problems of propagation and processing. In Marine Bio-Acoustics (ed. W. N.
Tavolga), pp. 87-100. Oxford: Pergamon.
PARVULESCU, A. (1967). The acoustics of small tanks. In Marine Bio-Acoustics, vol. 2(ed. W. N. Tavolga),
pp. 7-13. Oxford: Pergsmon.
PlDDlNQTON, R. W. (1972). Auditory discrimination between compressions and rarefactions by goldfish.
J. exp. Bio/. 56, 403-419.
POOGENDORF, D. (i9S2>. Die absoluten Horschwellen des Zweigwelses (Amiurus tiebulcsus) und Beitrfige
zur Physik des Weberscben Apparates der Ostariophysen. Z. vergl. Physicl. 34, 222-257.
POPPER, A. N. (1970). Auditory capacities of the Mexican blind cavefish (Astyanax jordani) and its eyed
ancestor (Astyanax mexicanus). Anim. Behav. 18, 552-562.
POPPER, A. N. & TAVOLGA, W. N. (1981). Structure and function of the ear in the marine catfish, Arius
felis. J. comp. Physiol. (In the Press.)
SCHARF, B. (1961). Complex sounds and critical bands. Psychol. Bull. 58, 205-217.
SCHARF, B. (1970). Critical bands. In Foundations of Modern Auditory Theory, vol. 1 (ed. J. V. Tobias)
pp. 157-202. New York: Academic.
TAVOLQA, W. N. (1962). Mechanisms of sound production in the ariid catfishes, Galeichthys and Bagre.
Bull. Am. Mus. Nat. Hist. 134, 1-30.
TAVOLGA, W. N. (1967). Masked auditory thresholds in teleost fishes. In Marine Bio-Acoustics, vol. 2
(ed. W. N. Tavolga), pp. 233-245. Oxford: Pergamon.
TAVOLGA, W. N. (1971 a). Acoustic orientation in the sea catfish, Galeichthys felis. Ann. N. Y. Acad. Sci.
188, 80-97.
TAVOLCA, W. N. (19716). Sound production and detection. In Fifh Physiology, vol. 5 (ed. W. S. Hoar
and D. J. Randall), pp. 135-205. New York: Academic
TAVOLOA, W. N. (1974). Signal/noise ratio and the critical band in fishes. J. Acoust. Soc. Am. 55,
I323-I333.
TAVOLGA, W. N. (1976 a). Recent advances in the study of fish audition. In Sound Reception in Fishes
(ed. W. N. Tavolga), pp. 37-52. Stroudsburg, Pa.: Dowden, Hutchinson & Ross.
TAVOLOA, W. N. (19766). Acoustic obstacle detection in the sea catfish (Arius felis). Sound Reception in
Fish (ed. A. Schuijf and A. D. Hawkins), pp. 185-204. Amsteidam: Elsevier.
TAVOLCA, W. N. (1977). Mechanisms for directional hearing in the sea catfish (Arius felis). J. exp. Biol.
67,97-115.
TAVOLOA, W. N. & WODINSKY, J. (1963). Auditory capacities in fishes. Pure tone thresholds in nine
species of marine teleosts. Bull. Am. Mus. Nat. Hist. ia6, 177-240.
TAVOLOA, W. N. & WODINSKY, J. (1065). Auditory capacities in fishes: Threshold variability in the
blue-striped grunt, Haemulon tciurus. Anim. Behav. 13, 301—311.
VAN BERGEIJK, W. A. (1967). Discussion of critical bands in fishes. In Marine Bio-Acoustics, vol. 2
(ed. W. N. Tavolga), pp. 244-245. Oxford: Pergamon.
VON BBKBSY, G. (i960). Experiments in Hearing. New York: McGraw-Hill.
WEVHR, E. G. (1969). Cochlear stimulation and Lempert's mobilization theory. Archs. Otolar. 90, 63.
WILSON, J. P. (1967). Psychoacoustics of obstacle detection using ambient or self-generated noise. In
Animal Sondr Systems (ed. R.-G. Busnel), pp. 89-114. N.A.T.O. Advanced Study Institute.
WINN, H. E., MARSHALL, J. A. & HAZLBTT, B. A. (1964). Behavior, diel activities, and stimuli that elicit
sound production and reaction to sounds in the longspine squirrelfish. Copeia 1964, 413—425.