Temporal Auditory Summation in the Black Sea Bottlenose Dolphin
G. L. Zaslavskiy
University authority for applied research, Ramot, Tel-Aviv
zaslg@bezeqint.net
Abstract
Absolute and masked thresholds for a tone pulse, a
broadband click and a double click were measured in
the Black Sea bottlenose dolphins as a function of the
pulse duration, the pulse or click repetition time, and
interval between the first and second clicks of the
double click, respectively. Estimates of the auditory
integration time in the bottlenose dolphins ranged from
around 0.5 to 2 ms for different signal types. The
auditory temporal summation was found to be the same
at frequencies from 10 to 135 kHz.
1. Introduction
The phenomenon of temporal auditory summation - an
increase in the auditory sensitivity with an increase in
the duration of a tone pulse – was attributed in humans
to the auditory energy integration [1]. The integration
time constant in the Atlantic bottlenose dolphin was
found to change with frequency from 200 ms at 4 kHz
to 40 ms at 45 kHz [2]. Johnson [2] suggested that
dolphins integrated pure-tone acoustic energy in the
same way as humans although he considered his data
for a 100-kHz tone pulse to be inconclusive.
However, the most effective summation in the Black
Sea bottlenose dolphin occurred at a click repetition rate
higher than 2000 Hz [3], which correspond to an
integration time constant of around 0.5 ms. The same
integration time of 0.5 ms was estimated for a double
click [2]. The double click absolute threshold was
measured as a function of the interclick interval. A
slightly shorter integration time constant of 0.264 ms for
a double click was found in the Atlantic bottlenose
dolphin [4].
The integration time of 0.264 ms was attributed to
the auditory analysis of broadband brief signals [4]. The
bottlenose dolphin is believed to process broadband
clicks and narrow-band tone-like signals with two
different – short (0.25- 0.3 ms) and long (dozens of
milliseconds) - integration time constants [4, 5].
Masked thresholds for a periodic 60-kHz tone pulse
with 0.025 to 1.6-ms duration were measured in the
beluga whale [6]. The integration time increased almost
directly with the tone pulse duration from 0.05 ms for a
0.025-ms pulse to 8 ms for a 1.6-ms pulse. Johnson
found it difficult to describe the single pulse thresholds
for the beluga whale with some theoretical function of
Th4.C2.1 IV - 2733
the pulse duration. He compromised on the integration
time of 20 ms and critical bandwidth of 1000 Hz. The
results suggested that signal integration in the beluga
whale was very much different from that in the
bottlenose dolphin [2].
The objective of the present study was to investigate
auditory temporal summation of tone pulses, broadband
clicks, and double clicks in the Black Sea bottlenose
dolphin. Absolute and masked thresholds were
measured as a function of the tone pulse duration, the
click repetition time, and interval between the first and
second clicks of the double click.
2. Methods
The subjects were adult Black Sea bottlenose dolphins
(Tursiops truncatus). Experiments were conducted in a
28 × 13 × 4 m concrete pool. The two-response forced-
choice procedure was used. A vertical net partition
between two transducers set a minimum distance of 3m,
from which the dolphin was to make its choice. A signal
was presented through one of the transducers situated on
either side of the partition at 1m depth and 3 m from
each other. Spherical transducers (1.2 cm in diameter)
were used for transmitting of broadband clicks and tone
pulses at frequencies from 100 to 150 kHz. The
maximum of the transducer transmitting response was at
110-120 kHz. 10, 20 and 50-kHz tone pulses were
transmitted through cylindrical magnetostrictive
transducers (20 cm in height and 6 cm in diameter),
with a relatively flat transmitting response (within 6 dB)
over a frequency range from 10 to 80 kHz. All
calibrations were made using a B&K hydrophone model
8103.
Prior to stimuli presentation, the dolphin positioned
itself at the far (from the transducers) end of the
partition. The dolphin was required to approach the
transducer, which was transmitting a signal. The choice
of which transducer would be transmitting at a given
trial was randomized. In order to measure masked
thresholds, a broadband continuous noise was
transmitted through both transducers. The signal was
randomly mixed with a broadband noise at one of the
transducers. The level of the noise was around 26 dB
above the dolphin’s absolute threshold for the noise.
The threshold measurements were made using a method
of constant stimuli. Near the threshold, the amplitude
was changed by a 2-dB step in 10-trails blocks. The
threshold was reached 2 to 4 times during a session. The
animals performed 200 to 300 trials per session. A
threshold estimate was completed when over at least 2
consecutive sessions threshold values were within 3 dB
of each other. The threshold values from these sessions
were averaged for the threshold estimate at a 75%
correct response level.
In the first series of experiments, absolute and
masked thresholds were measured as a function of the
tone-pulse duration at frequencies 50, 100, 130, 135,
137, 140 and 150 kHz. The pulse repetition rate was 2-3
Hz.
In the second series of experiments, absolute and
masked thresholds for a broadband click and a tone
pulse were measured as a function of the signal
repetition time. The peak frequency of the click was
between 110 and 130 kHz. 10-, 20-, and 100-kHz tone
pulses were tested. The duration of the low frequency
tone pulses was 0.1 ms. The thresholds at 100-kHz were
measured for a 0.05- and 1-ms tone pulse duration.
Finally, auditory thresholds for a double click and a
double pulse were measured as a function of the
separation time between the clicks and between the
pulses. The double click was comprised of the
broadband clicks. The double pulse consisted of 100-
kHz tone pulses with duration of 0.06 ms.
3. Results
3.1. Tone pulse
As the tone pulse duration was increased from 0.2 to
around 2 ms, the threshold decreased by more than 20
dB at a rate of 3 – 4 dB per doubling of the duration
(Fig. 1).
150 kHz 140 kHz 137 kHz
135 kHz 130 kHz 100 kHz
50 kHz
50
40
Threshold (dB)
30
20
10
0 100ms by only 2-3 dB per decade (Fig. 3). A similar
0.01 0.1 1 10 100
Pulse duration (msec)
Figure 1. Absolute thresholds for a tone pulse versus the pulse
duration. 0 dB corresponds to the absolute threshold for a 100-
kHz pure tone. Dolphin TM78-90. The frequencies of the tone
pulses are shown in the legend.
At a further increase in the pulse duration from 1 to
1000 ms, the threshold decreased by less than 10 dB.
The longest pulse for which the threshold change was
IV - 2734
close to the energy summation gives the estimate of the
dolphin’s auditory integration time constant of around 2
ms.
There was a somewhat reversed summation effect at
150 kHz; the threshold slightly increased with the
increase in the duration (Fig. 1, 150 kHz). The temporal
summation was pronounced at frequency as high as 135
kHz but significantly degraded at higher frequencies.
The presence of temporal summation can be an
indication of whether the frequency of a tone pulse is
within the frequency range of the dolphin’s hearing.
Above 135 kHz, the dolphin may lose its ability for
auditory analysis of signals and probably detected the
broad band transients of the pulses. It was found that the
dolphin retained frequency discrimination ability up to
130 kHz [7]. Frequency difference limens significantly
increased only at 140 kHz which indicated
approximately the same auditory upper frequency limit
that we found for the temporal summation.
The absolute and masked thresholds for a tone pulse
changed with the pulse duration in a similar manner
(Fig. 2). Proportionally to the noise level, the masked
thresholds shifted to a higher level relative to the
absolute thresholds.
100 kHz 100 kHz, masked threshold
50
40
Threshold (dB)
30
20
10
0
0.01 0.1 1 10 100
Pulse duration (msec)
Figure 2. Absolute and masked thresholds for a 100-kHz tone
pulse versus the pulse duration. 0 dB corresponds to the
absolute threshold for a 100-kHz pure tone. Dolphin TL77-79.
3.2. Periodic clicks and tone pulses
As the repetition time was increased from 0.03 to 0.5-
1ms, the absolute and masked thresholds for clicks rose
by 4 to 5 dB per doubling and further from 0.5 ms to
threshold change was observed for a 0.05-ms tone pulse
(Fig. 3, 100 kHz, 0.05-ms pulse). Taken at the
intersection of a steep and a slow threshold change with
the click repetition time, the integration time estimates
are between 0.5 and 1 ms (Fig. 3 and 4).
Temporal summation for a 1-ms pulse was observed
only when a repetition time was decreased from 2 to 1
ms (Fig. 4). This agrees with the 1 to 2-ms integration
time estimate yielded by the threshold dependence on
the tone pulse duration (Fig. 1). The 1-ms tone pulse
was almost fully integrated to the maximum auditory
response even at the largest tested repetition time of 100 superimposed the curves although one of them was the
ms. absolute threshold and two others were the masked
TP72-78, Zanin et al. 1977
thresholds for different noise levels.
TL77-79, masked threshold
TL77-79, absolute threshold TP72-78, absolute threshold, Zanin et al. 1977
50 Masked threshold, Au et al. 1988
TL77-79, masked threshold, 0.06 ms, 100 kHz
40
Threshold (dB)

1
30 0

Threshold (dB)
-1
20
-2
10 -3
-4
0
-5
0.01 0.1 1 10 100
0.01 0.1 1 10
Repetition time (msec)
Interval (msec)
Figure 3. Absolute and masked thresholds for a click versus
the click repetition time. Figure 5. Absolute and masked thresholds for a double click
and double pulse versus interval between clicks and between
100-kHz tone pulses. The duration of the tone pulses was 0.06
TL77-79, 100 kHz, 1 ms, masked threshold
ms. 0 dB corresponds to threshold for a single click and a
TL77-79, 100 kHz, 0.05 ms, masked threshold
single 0.06- ms tone pulse.
TM78-90, 20 kHz, 0.1 ms
TM78-90, 10 kHz, 0.1 ms
The integration times estimated in the Black Sea
50 bottlenose dolphin were found to be much smaller than
that measured in the Atlantic bottlenose dolphin [2].
40 However, the thresholds for the Black Sea bottlenose
Threshold (dB)

dolphin changed with the pulse repetition time

30
20
10
0 ms. Johnson [6] used a simple energy detector model to
0.1 1 10
Repetition time (msec)
Figure 4. Absolute and masked thresholds for a tone pulse
versus the tone pulse repetition time. 0 dB corresponds to the
absolute threshold for a 100-kHz pure tone. Frequency and
duration of tone pulses are shown in the legend.
The biggest surprise was the 1-ms integration time
observed for tone pulses at the 10- and 20-kHz audio
frequencies (Fig. 4, 10 and 20 kHz, 0.1 ms).
3.3. Double click
The double click absolute threshold as a function of
the interclick interval is shown in Fig. 5. The temporal
summation of the double-click continued up to 1 ms.
For the double-pulse consisting of the 0.06-ms tone
pulses, the summation interval was around 0.5 ms (Fig.
5, dolphin TL, 0.06 ms, 100 kHz). Our data showed a
slightly larger auditory integration time than was found
for a Atlantic bottlenose dolphin [4], which can be
attributed to individual differences between the
dolphins. In order to compare the results, we
practically in the same proportion as in the beluga whale
[6]. The only difference was that instead of the abrupt
threshold jump at large repetition times found in the
beluga whale, the bottlenose dolphin thresholds very
slowly increased as a repetition time increased beyond 1
100 analyze the results and found that the integration times
for 0.1, 0.3 and 0.8-ms pulse were 0.4, 0.9 and 2.8 ms,
respectively. These estimates of the integration times for
the beluga whale are nearly within the range of the
integration times found for the bottlenose dolphin in our
experiments. The exceptions were the integration times
found in the beluga whale for the shortest (0.025 ms)
and longest (1.6 ms) pulses.
The threshold change of 4 - 5 dB per doubling of the
tone pulse duration or repetition time was steeper than
what an energy detector would show, and suggests
involvement of the auditory filter in signal processing
[6]. There is approximately twofold difference in the
integration time estimate for broadband clicks (0.5 to 1
ms) and tone pulses (1 to 2 ms). The longer integration
time for the tone pulses could be attributed to the
analysis with auditory filters. At present, however, we
would rather make only a simple and assured conclusion
that whatever caused the auditory summation in the
bottlenose dolphin, it significantly diminished beyond a
time interval of 0.4 to 2ms.
The bottlenose dolphins’ thresholds for a periodic
pulse differed from the thresholds measured in the

IV - 2735
beluga whale for a single pulse [6]. However, the latter
were also different from the beluga whale’s thresholds
for a periodic pulse [6]. Obviously, the dolphin had to
be very attentive in order to pick up a single pulse,
especially a short one. The beluga whale had no chance
to try again, as it always could do in case of a periodic
pulse even at a long repetition time. Vel’min [8] found
that in the range of the click repetition rates between 1
to 6 Hz, the shift in threshold was 8 dB and 12 dB for
two dolphins. However, for one of those dolphins we
later found no threshold change within click repetition
rate from 1 to 10 Hz [3]. The dolphin learned to be more
attentive to a short click, which resulted in significant
reduction in the thresholds at very low repetition rates.
The differences in thresholds for a single pulse and for a
periodic pulse of the same duration found in the beluga
whale [6] could be attributed to the same phenomenon.
Moreover, the tone pulse thresholds in the Atlantic
bottlenose dolphin [2] were also measured for a single
pulse. It might be that if instead of a single pulse, a
periodic pulse has been used, the dolphin would have
shown much shorter integration time, similar to that
revealed in our experiments with the Black Sea
bottlenose dolphin.
the bottlenose dolphin. 9th All-Union Acoust. Conf.,
Moscow, pp. 21-23, 1977.
[4] Au, W.W.L., Moore, P.W.B., and Pawloski,
D.A.”Detection of complex echoes in noise by an
echolocating dolphin.” J. Acoust. Soc. Am. 83: 662-668.
1988.
[5] Dubrovskiy, N. A. “On the two auditory subsystems
of dolphins,” in: Sensory Ability of Cetacean:
Laboratory and Field Evidence, edited by J. A. Thomas
and R. Kastslein, Plenum Press, pp. 233-254, 1990.
[6] Johnson, S. C. “Hearing thresholds for periodic 60-
kHz tone pulses in the beluga whale.” J. Acoust. Soc.
Am. 89 (6), 1991.
[7] Thompson, R. K. R., and L. M. Herman.
“Underwater frequency discrimination in the bottlenose
dolphin (1-140kHz) and the human (1-8),” J. Acoust.
Soc. Am. 57, 943-94, 1975.
[8] Vel’min, V. A., Titov, A.A., and Yurkevich, L.I.
”Time summation of pulses in the bottlenose dolphin,”
in: Aquatic mammals, Part 1. Kiev, Naukova Dumka,
pp. 78-80, 1975.
[9] Zaslavskiy, G. L. “Target echo processing in the
dolphin’s auditory system,” OCEAN 2003 MTS/IEEE,
conference proceedings, pp 620-628 2003.

4. Conclusions
For three different types of the signals - a periodic click,
a double click, and a tone pulse - the Black Sea
bottlenose dolphin’s thresholds produced very similar
integration time estimates between 0.5 and 2 ms. The
temporal summation significantly diminished above
frequency 135 kHz. This frequency is likely to be a high
frequency limit for auditory analysis in the bottlenose
dolphin. As far as temporal summation is concerned,
there were no much differences in the dolphins’
treatment of broadband clicks and narrow-band tone-
like signals. It should be mention, however, that the
bottlenose dolphin is able to considerably decrease the
auditory integration time to 0.02-0.03 ms [9]. We
observed such a short integration time in many
behavioral experiments, especially in signal
discrimination tasks.
The bottlenose dolphin integration time at 10 and 20
kHz of 1 ms is much shorter than the integration time of
around 200 ms at 10 kHz found for humans. The results
suggest that the auditory integration in the bottlenose
dolphin is very much different from that in humans even
at audio frequencies.

5. References
[1] Zwislocki, J. “Theory of temporal auditory
summation.” J. Acoust. Soc. Am. 32:1046-1060. 1960.
[2] Johnson, S.C. “Relation between absolute thresholds
and duration-of-tone pulses in the bottlenose dolphin,”
J. Acoust. Soc. Am. 43: 757-763, 1968.
[3] Zanin, A.V., Zaslavskiy, G.L., and Titov, A.A.
Temporal summation of pulses in the auditory system of

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