underwater detection of tonal signals between 0.125 and 100 khz by harbor seals (phoca vitulina)

Underwater detection of tonal signals between 0.125 and100 kHz by harbor seals (Phoca vitulina)

Ronald A. Kastelein,a� Paul J. Wensveen, and Lean HoekSea Mammal Research Company (SEAMARCO), Julianalaan 46, 3843 CC Harderwijk, The Netherlands

Willem C. VerboomAcoustic Consultancy, Junostraat 10, 2402 BH, Alphen a/d Rijn, The Netherlands

John M. TerhuneDepartment of Biology, University of New Brunswick, P.O. Box 5050, Saint John, New Brunswick E2L 4L5,Canada

�Received 19 May 2008; revised 30 October 2008; accepted 20 November 2008�

The underwater hearing sensitivities of two 1-year-old female harbor seals were quantified in a poolbuilt for acoustic research, using a behavioral psychoacoustic technique. The animals were trainedto respond when they detected an acoustic signal and not to respond when they did not �go/no-goresponse�. Pure tones �0.125–0.25 kHz� and narrowband frequency modulated �tonal� signals�center frequencies 0.5–100 kHz� of 900 ms duration were tested. Thresholds at each frequencywere measured using the up-down staircase method and defined as the stimulus level resulting in a50% detection rate. The audiograms of the two seals did not differ statistically: both plots showedthe typical mammalian U-shape, but with a wide and flat bottom. Maximum sensitivity �54 dB re1 �Pa, rms� occurred at 1 kHz. The frequency range of best hearing �within 10 dB of maximumsensitivity� was from 0.5 to 40 kHz �6 1

3 octaves�. Higher hearing thresholds �indicating poorersensitivity� were observed below 1 and above 40 kHz. Thresholds below 4 kHz were lower thanthose previously described for harbor seals, which demonstrates the importance of using quietfacilities, built specifically for acoustic research, for hearing studies in marine mammals. The resultssuggest that under unmasked conditions many anthropogenic noise sources and sounds fromconspecifics are audible to harbor seals at greater ranges than formerly believed.© 2009 Acoustical Society of America. �DOI: 10.1121/1.3050283�

PACS number�s�: 43.80.Lb, 43.80.Nd �WWA� Pages: 1222–1229

I. INTRODUCTION

The harbor seal �Phoca vitulina� has the most extensivegeographic distribution of any seal species. It inhabits theeastern Baltic Sea as well as both eastern and western coastsof the Atlantic �30° to 80° north� and Pacific �28° to 62°north� Oceans. It leads an amphibious life, resting and pup-ping on land, while migration, foraging, and courtship occurunderwater �Burns, 2002�. During the breeding season, maleharbor seals produce underwater broadband pulsed vocaliza-tions, termed roars, that have their major sound energy be-tween 0.4 and 2 kHz and durations of 1–10 s �Schustermanet al., 1970; Van Parijs and Kovacs, 2002�.

To determine the importance of sound for harbor sealsduring activities such as communication, reproduction,predator avoidance, and navigation, and the potential for dis-turbance by anthropogenic noise, information is needed onthe species’ underwater hearing sensitivity. This has beentested for pure tones �Møhl, 1968; Terhune, 1988, 1989;Turnbull and Terhune, 1993; Kastak and Schusterman, 1998;Southall et al., 2005� and frequency swept tones �Turnbull

a�Author to whom correspondence should be addressed. Electronic mail:
[email protected]
1222 J. Acoust. Soc. Am. 125 �2�, February 2009 0001-4966/2009/1

and Terhune, 1994�. However, in each of the seven studies,only the sensitivity of a single harbor seal over a part of thefrequency range of hearing was investigated. Moreover, ineach study different equipment, methodology, and signal pa-rameters were used and the animals were of different ages�but all were males�. In addition, some of the hearing thresh-olds may have been influenced �masked� by backgroundnoise in the research pool. Because of the differences inthese studies it is difficult to construct an appropriate com-posite audiogram to describe the hearing capabilities of har-bor seals.

Many human activities occur in the coastal waters whereharbor seals are found. To assess potential disturbance byanthropogenic noises, it is important to obtain robust under-water hearing threshold curves for this pinniped species. Forthis, a quiet testing environment and multiple representativestudy animals are needed. Therefore, a pool and filtrationsystem with special acoustic features designed for hearingstudies was built at a quiet location in the Netherlands. Twoyoung healthy female harbor seals were obtained specificallyfor this hearing study. Our aim was to determine absolute�unmasked� underwater hearing thresholds for both seals
over their entire hearing range.
© 2009 Acoustical Society of America25�2�/1222/8/$25.00

II. MATERIALS AND METHODS

A. Study animals

The study animals were two female harbor seals �iden-tified as SM.Pv.01 and SM.Pv.02�, which were born at Eco-mare, Texel, The Netherlands. The animals were moved tothe research facility soon after they had been weaned.Throughout the study, the animals were healthy. They werenot exposed to ototoxic medication prior to or during thestudy period. During the study they aged from14 to 18 month old and their body weight increased fromaround 34 to around 42 kg. The seals consumed between 1.4and 1.8 kg of thawed fish �herring, Clupea harengus, mack-erel, Scomber scombrus, and sprat, Sprattus sprattus� di-vided into four meals per day. In general, the seals receivedmost of their daily ration during research sessions.

B. Study area and staff

The study was conducted at SEAMARCO’s ResearchInstitute, The Netherlands, which is in a remote area that wasspecifically selected for acoustic research. The measurementswere conducted in an outdoor pool �8 m�l��7 m�w�, 2 mdeep�, with an adjacent haul-out platform �Fig. 1�. The poolwalls and floor were made of plywood covered with polyes-ter. The pool floor was 1 m below ground level. To reducesound reverberation in the pool, the inner walls were covered

FIG. 1. The study area, showing the test harbor seal in position at theunderwater listening station, and the nontest animal with the other trainer;�a� top view and �b� side view, both to scale.

with 3-cm-thick mats of coconut fiber embedded in

J. Acoust. Soc. Am., Vol. 125, No. 2, February 2009

4-mm-thick rubber. The coconut mats extended 10 cm abovethe water level to reduce splashing noises caused by waves.The bottom of the pool was covered with approximately20 cm of sand. Skimmers kept the water level constant. Sea-water was pumped in directly from the nearby Ooster-schelde, a lagoon of the North Sea. Most of the water �80%�was recirculated daily through a biological filter system toensure year-round water clarity, so that the animals’ behaviorcould be observed via an underwater camera during the testsessions.

To limit the amount of noise that the seals were exposedto on a regular basis �to prevent a temporary hearing thresh-old shift before the hearing tests�, the water circulation sys-tem and aeration system for the adjacent biofilter were de-signed to be as quiet as possible. This was done by choosing“whisper flow” pumps, mounting the pumps on rubberblocks, and connecting the pumps to the circulation pipeswith very flexible rubber hoses. There was no current in thepool during the experiments, as the water circulation pumpand the air pump of the biofilter were switched off for10 min before and during test sessions. This also preventedflow noise from the skimmers. The water temperature variedbetween 20 °C in August and 12 °C in November, and thesalinity was around 3.4%.

During the 15 min test sessions the animal not beingtested was trained to keep very still in the water next to thehaul-out area �this was quieter than staying on land, where ascratch of a flipper nail could trigger a prestimulus responsein the animal being tested�. The signal operator and theequipment used to produce the stimuli and listen to under-water sounds were in a research cabin next to the pool, out ofsight of the animals �Fig. 1�.

C. Test stimuli

A schematic of the equipment used to configure and emitoutgoing signals is shown in Fig. 2. All stimuli were pro-duced by a waveform generator �Hewlett Packard, model33120A�. Two types of tonal signals were used. Between0.125 and 0.25 kHz, pure tones were used because due to thesize of the pool the chances of standing waves occurring

FIG. 2. Block diagram of the transmitting and listening systems.

were small for these long wavelengths. Between 0.5 and

Kastelein et al.: Harbor seal underwater audiogram 1223

100 kHz, narrowband sinusoidal frequency-modulated �FM�tonal signals �with center frequencies of 0.5, 1, 2, 4, 8, 16,25, 31.5, 40, 50, 63, 80, and 100 kHz� were used. The modu-lation range of the signals was �1% of the center frequency�the frequency around which the signal fluctuated symmetri-cally�, and the modulation frequency was 100 Hz �for ex-ample, if the center frequency was 10 kHz, the frequencyfluctuated 100 times per second between 9.9 and 10.1 kHz�.Narrowband FM signals were used above 0.25 kHz becausesuch signals produce fewer constructive and destructive in-terference effects �standing waves� in a reverberant pool thanpure tones �Kastelein et al., 2002, 2005; Finneran andSchlund, 2007�.

A modified audiometer for testing human aerial hearing�Midimate, model 602� was used to control the duration andamplitude of signals. The stationary portion of all signalswas 900 ms in duration; the rise and fall times were 50 ms toprevent transients. Hearing thresholds depend on signal du-ration, and integration time is also frequency dependent, de-creasing with increasing frequencies �Terhune, 1988�. The900 ms signal duration used in the present study is probablyabove the integration time of the harbor seal’s hearing sys-tem. The sound pressure level �SPL� at the seal’s head whileit was at the listening station could be varied in 5 dB incre-ments �this step size was determined by the audiometer:5 dB steps are generally used in human audiometry�. The0.125–0.5 kHz signals from the audiometer were amplifiedby means of an audio amplifier �Sony TA-F335 R�.

A directional transducer �Ocean Engineering Enterprise,model DRS-12; 30 cm diameter� was used to project the sig-nals into the water �an impedance matching transducer wasnot used, in order to eliminate harmonics�. Multipath arrivalsand standing waves can introduce both temporal and spatialvariations in the observed SPL at the listening station. There-fore, the transducer was placed in a corner of the pool in aprotective wooden box lined with sound-absorbing rubber.The transducer was hung with four nylon cords from thecover of the box and made no contact with the box. A stain-less steel weight was fixed to the lower part of the transducerto compensate for its buoyancy. The transducer was 1.85 mfrom the tip of the L-shaped listening station �Fig. 1�, andwas positioned so that the acoustic axis of the projectedsound beam pointed at the center of the listening station �i.e.,the center of the study animal’s head while it was at thelistening station�. To reduce reflections from the bottom ofthe pool and water surface reaching the listening station, abaffle board was placed halfway between the transducer andthe animal. The board consisted of 2.4 m high, 1.2 m wide4 cm thick plywood, covered with a 2 cm thick closed cellrubber mat on the side facing the transducer. A 30-cm-diameter hole was made in the board with its center at thesame level as the seal’s head and the transducer �1 m belowthe water surface�. As an indicator of the condition of thetransducer, its capacitance was checked once a week with acapacity meter �SkyTronic 600.103�. During the study period
the capacity remained constant.
1224 J. Acoust. Soc. Am., Vol. 125, No. 2, February 2009

D. Stimuli level calibration and background noisemeasurement

Audiograms are easily influenced by background noisein the test area. Therefore, great care was taken to make theseal’s listening environment as quiet as possible. Nobodywas allowed to move within 15 m of the pool during ses-sions. Underwater background noise levels were measuredmonthly during the study period, under the same conditionsas during the test sessions �i.e., in various weather conditionsbut without rain and with wind speed below Beaufort 3�.

The equipment used to measure the background noise inthe pool consisted of a hydrophone �Bruel & Kjær �B&K�8101�, a voltage amplifier system �TNO TPD, 0–300 kHz�,and a dual spectrum analyzer system �0.025–160 kHz�. Thesystem was calibrated with a pistonphone �B&K 4223� and awhite noise signal �0.025–40 kHz� which was inserted intothe hydrophone preamplifier. Measurement results were cor-rected for the frequency sensitivity of the hydrophone andthe frequency response of the measurement equipment. Thecustomized analyzer consisted of an A/D-converter �AvisoftUltraSoundGate 116; 0–250 kHz� coupled to a notebookcomputer �sampling rate: 500 kHz�. The digitized recordingswere analyzed by two parallel analysis systems: �1� a fastFourier transform narrow-band analyzer �0.025–160 kHz�and �2� a 1 /3-octave band analyzer �0.025–160 kHz�.

1 /3-octave band background noise levels were deter-mined in the range 0.025–100 kHz and converted to‘equivalent sound pressure spectrum levels’ �Leq method,Hassall and Zaveri, 1988�, expressed in dB re 1 �Pa / �Hz.Figure 3�a� shows the power averaged �n=5� backgroundnoise in the pool, alongside the self-noise of the measuringsystem.

The received SPL �dB re 1 �Pa, rms� of each stimuluswas measured approximately once each month at the seals’head position �Fig. 1�. During trials, the seals’ head positions�while at the listening station� were carefully monitored andwere consistent to within a few cm. The received SPL varia-tion between calibration sessions was frequency dependent.The deviation from the mean was generally around 2 dB forall frequencies, except 31.5 kHz, where for unknown reasonsthe deviation from the mean was around 5.5 dB. No har-monic distortions were present in the test frequencies at theSPLs used in the hearing tests. The linear averaged receivedSPL per test frequency was calculated from all five calibra-tion sessions. The means were used to determine the sessionthresholds.

The received SPLs were calibrated at a level of14–65 dB �depending on frequency� above the thresholdlevels found in the present study. The linearity of the trans-mitter system was checked during the study by measuringlevels around 15 dB above the thresholds found in this study,and it was consistent within a few decibels. At one frequency�0.125 kHz� the stimulus tone levels could not be amplifiedsufficiently above background noise to ensure that the mea-surements were not influenced by the background noise. TheSPL was also measured 10 cm in all directions from the lis-
tening station �the location of the seal’s head�, and varied
Kastelein et al.: Harbor seal underwater audiogram

between 0 and 4 dB �depending on the frequency� from theaverage SPL used to calculate the thresholds.

E. Experimental procedure

The seals were trained to respond �“go”� in the presenceof a signal and to withhold the response �“no-go”� in the

FIG. 3. �a� Power averaged background noise level in the pool in dB re1 �Pa / �Hz �derived from 1/3-octave band levels; n=5� and the self-noiseof the B&K 8101 hydrophone �amplifier�. Also shown are noise levels at seameasured at sea states 0 and 2 �Knudsen et al., 1948�. �b� The mean 50%detection thresholds �dB re 1 �Pa, rms, line level� for pure tone and nar-rowband FM �900 ms� signals obtained for female harbor seals 01 �� and02 �� in the present study �for details see Table I�. The thin line shows thecalculated noise-limited theoretical detection threshold �dB re 1 �Pa� basedon the background noise levels of Fig. 3�a� and CRs of harbor seal hearing.�c� The average underwater hearing threshold �in dB re 1 �Pa, rms� of thetwo study animals in the present study, shown as a line, and the underwaterhearing thresholds found for harbor seals in previous studies �Møhl, 1968��500 ms, ��; Terhune, 1988 �500 ms, ��; Turnbull and Terhune, 1993�repeated signals, 50 ms, 10/s, ��; Kastak and Schusterman, 1998 �500 ms,��; Southall et al., 2005 �500 ms, ��. The numbers between brackets in-dicate the signal durations used in the studies

absence of a signal. A trial began when the nonstudy animal


was near the platform with one trainer and the study animalpositioned with its head at the start/response buoy at the edgeof the pool next to the research trainer �Fig. 1�a��. When thetrainer gave the animal a vocal command accompanied by agesture �pointing downwards�, the animal descended to thelistening station �an L-shaped, 32-mm-diameter, water-filledpolyvinylchloride tube with an end cap�, so that its externalauditory meatus was 200 cm from the sound source and100 cm below the water surface �i.e., midwater; Fig. 1�b��.Each animal was trained to position its nose against the lis-tening station so that its head axis was in line with the pro-jected beam axis of the transducer. The listening station wasnot connected to the sound box, and the transducer was sus-pended within the box by four thin ropes, so the animalswere not able to use vibration via contact conduction to thenose to detect the signals. The animals’ positions could beviewed from above by means of an underwater camera�Mariscope, Micro�, which was attached to the listening sta-tion. The images were visible to the trainer near the start/response buoy �but out of the study animal’s view when itwas at the listening station� and to the operator in the re-search cabin.

Two trial types were conducted during each experimen-tal session: signal-present trials and signal-absent trials. Insignal-present trials, the stimulus was presented unpredict-ably between 4 and 10 s after the animal was positionedcorrectly at the listening station. A minimum waiting time of4 s was chosen because it took about 4 s for the waves,created by the animal’s descent, to dissipate. If the animaldetected the sound, it responded by leaving the listening sta-tion �go response� at any time during the signal’s durationand returning to the start/response buoy �Fig. 1�a��. The sig-nal operator then indicated to the trainer that the responsewas correct �a hit�, after which the trainer gave a vocal signaland the seal received a fish reward. If the animal did notrespond to the signal, the signal operator signaled to thetrainer that the animal had failed to detect the signal �a miss�.The trainer then indicated to the animal �by tapping softly onthe side of the pool� that the trial had ended, thus calling theanimal back to the start/response buoy. No reward was givenfollowing a miss. If the animal moved away from the listen-ing station to the start/response buoy before a signal wasproduced �a prestimulus response�, the signal operator indi-cated to the trainer to end the trial without rewarding theanimal. After a prestimulus response, the animal was ignoredfor 8–10 s by the trainer.

In signal-absent, or catch, trials the signal operator handsignaled to the trainer to end the trial after a random intervalof 4–10 s from when the seal had stationed �determined by arandom number generator�. The trial was terminated whenthe trainer blew very softly on a whistle. The tapping on thepool wall and whistle blowing were done softly to reduce theseal’s exposure level difference between the test signals andthe acoustic signals from the trainer. We believe this helpedthe animal to focus on very faint sounds throughout the ses-sions. If the animal responded correctly by remaining at thelistening station until the whistle was blown �a correct rejec-tion�, it then returned to the start/response buoy and received
a fish reward. If the seal left the listening station before the

whistle was blown �a prestimulus response�, the signal op-erator indicated to the trainer to end the trial without reward-ing the animal. The same amount of fish was given as areward for correct go and no-go responses. In both signal-present and signal-absent trials, the trainer was unaware ofthe trial type when she sent the animal to the listening sta-tion. After sending the animal to the listening station, thetrainer stepped out of the seal’s view.

A session generally consisted of 30 trials per animal andlasted for about 15 min per animal. The seals were alwaystested in the same order, one immediately after the other.Sessions consisted of 70% signal-present and 30% signal-absent trials presented in random order, and only one signalfrequency was presented each day. For each session, one offour data collection sheets was used. Each sheet comprised adifferent random series of trial types. Each seal had its ownset of four data collection sheets. In each session, the signalamplitude was varied according to the simple up-down stair-case procedure, a conventional psychometric technique�Robinson and Watson, 1973�. This is a variant of the methodof limits, which results in a 50% correct detection threshold�Levitt, 1971�. During preliminary sessions, a rough thresh-old per test frequency was determined. During subsequentexperimental sessions, the starting SPL of the signal was10–15 dB above the estimated threshold. Following each hit,the signal amplitude on the next signal-present trial was re-duced by 5 dB. Following each miss, the signal level wasincreased on the next signal-present trial by 5 dB. Prestimu-lus responses did not lead to a change in signal amplitude forthe next trial. A switch in the seal’s response from a detectedsignal �a hit� to an undetected signal �a miss�, or vice versa,is called a reversal.

Thresholds were determined for 16 tonal signals �threepure tones and 13 narrowband FM signals�. To prevent theanimals’ learning process from affecting the threshold levels,the test frequency was varied each day and adjacent frequen-cies were usually tested on successive days �going from lowto high and from high to low frequencies, and so forth�. Thisway the difference in frequency between days was limited,reducing the potential need for the study animals to adapt toa frequency. During the study we learned that the thresholdsobtained for higher frequencies ��40 kHz� were not influ-enced by the wind force. Therefore, those frequencies weretested under relatively high wind force conditions, whereasthe 0.125–0.5 kHz signals were only tested under wind forceconditions below 2 Beaufort, because they required a quieterenvironment. Usually four experimental sessions were con-ducted on 5 days per week �at 0900, 1100, 1400, and1600 h�. Data were collected between August and November2007.

Before each session, the acoustic equipment producingthe stimuli was checked to ensure that it was functional andthe stimuli were produced accurately �Fig. 2�. Also the back-ground noise level was checked to make sure it was not toohigh for testing. This was done in the following ways:

�1� To test the sound generating and amplifying equipment,the voltage output toward the underwater transducer was
measured with an oscilloscope �Dynatek 8120, 20 MHz;

Channel I� and a voltmeter �Hewlett Packard 3478A�.This was done with the stimulus to be used in that ses-sion, at the amplitude at which the stimuli were cali-brated.

�2� To test the sound level produced by the underwatertransducer, the voltage output of a hydrophone �Labforce1 BV�, which was always placed in a fixed position20 cm from the transducer and connected to a preamp-lifier �100� �, was checked with the same oscilloscope�Channel II� and voltmeter when the stimulus for thatsession was produced.

�3� Audio stimuli �at sufficient SPLs� were checked aurallyby the signal operator via another hydrophone �Labforce1 BV�, a charge amplifier �Bruel & Kjær, 2635�, and anamplified loudspeaker. The operator also used this setupto monitor the background noise aurally before and dur-ing each session.

�4� Ultrasonic stimuli ��16 kHz�; at sufficient SPLs� werechecked for via the hydrophone �Labforce 1 BV�. Thesignals were made audible to the signal operator bymeans of a modified ultrasound detector �Stag Electron-ics, Batbox III�.

F. Analysis

Sessions with more than 20% prestimulus responses�i.e., more than six of the usual 30 trials per session� werenot included in the analysis. These sessions occurred onlyfour times per animal during the entire study, and usuallycoincided with obvious transient background noises.

For each session, the mean session hearing thresholdwas calculated by taking the mean of all reversal pairs in thatsession. Because no warm-up trials were used, it sometimestook several reversals before a stable threshold was reached.In these cases, the first one to four reversal pairs were notincluded in the analysis. The data included in the final analy-sis were from sessions carried out after the mean sessionthreshold had leveled off. This usually occurred within foursessions �depending on the frequency and the animal�. Thereported thresholds for each seal were based on the mean ofall remaining reversal pair values per frequency; approxi-mately 110 reversal pairs per frequency obtained in about 11sessions. The hearing thresholds of the two seals at eachfrequency were compared using a paired t-test.

III. RESULTS

The seals’ sensitivity for each test frequency was stableover the 4 month study period. The mean prestimulus re-sponse rate �for both signal-present and signal-absent trials�varied between 3% and 13%, depending on the frequency�Table I�. Most prestimulus responses occurred during testswith low-frequency signals.

The thresholds of the two seals were similar �t=0.73,d . f . =15, P=0.48�. The underwater audiograms �50% detec-tion thresholds� for the two seals showed the typical mam-malian U-shape. However, the bottom part of the U was veryflat and wide, the low frequency sensitivity decreased gradu-ally, and the high frequency cutoff was steep �Fig. 3�b� and
Table I�. The range of best hearing �10 dB from the maxi-

mum sensitivity at 1 kHz which was 54 dB re 1 �Pa, rms�was very wide: from 0.5 to 40 kHz �6 1

3 octaves�, and sensi-tivity fell below 1 kHz and above 40 kHz.

IV. DISCUSSION AND CONCLUSIONS

A. Evaluation of the data

The biggest challenge in hearing studies is to maintain alow background noise level; we took great care to do this inthe present study. The main factor influencing the low-frequency part of the background noise spectrum in the poolwas the wind �which, when increased, caused airborne windnoise and increased soil vibrations�. During the 4 monthstudy period, the wind speed was low compared to otheryears, which resulted in very low background noise levels inthe pool �even partly below sea state 0, see Fig. 3�a��.

It is important to know whether the audiograms of thepresent study are absolute audiograms or if the signals wereinfluenced by the background noise in the pool. Theoreticalmasked detection thresholds �MDTs� �Fig. 3�b�� were calcu-lated based on the mean background noise levels �Fig. 3�a��and the harbor seal’s critical ratio �CR� �from a smooth linethrough the data points of Turnbull and Terhune, 1990 andSouthall et al., 2000; Table I�. The noise-limited theoreticalMDT is calculated as MDT=background noise �spectrumlevel�+CR. The theoretical MDTs lie below the hearingthresholds found in the present study, suggesting that thethresholds were not masked by the ambient noise. Also, thebackground noise measurements averaged the sound pres-

TABLE I. The mean 50% detection thresholds, stand1-year-old female harbor seals 01 and 02 for three�0.5–100 kHz� signals, and their prestimulus responstrials �signal-present and signal-absent trials�. Also shthreshold in Fig. 3�b�.

Centerfrequency

�kHz�

Frequencymodulationrange 1%of centerfrequency

�kHz�

Criticalratio�dB�

Harb

TotalNo. of

reversalpairs

Meandetethres

�SPLre 1 �P

�

0.125 Pure tone 14.6 126 770.200 Pure tone 14.6 112 720.25 Pure tone 14.7 116 650.5 0.495–0.505 14.8 93 611 0.99–1.01 15.2 128 542 1.98–2.02 16.3 100 574 3.96–4.04 19.0 126 568 7.92–8.08 22.0 120 61

16 15.84–16.16 25.0 118 6125 24.75–25.25 27.0 109 5731.5 31.19–31.82 28.0 108 6440 39.60–40.40 ¯ 102 6150 49.50–50.50 ¯ 120 7363 62.37–63.63 ¯ 112 10980 79.20–80.80 ¯ 106 119

100 99.00–101.00 ¯ 114 127

sure over time, whereas the level certainly fluctuated tempo-


rally. Most masking studies have been conducted with ran-dom Gaussian noise, but in the real world, the acousticenvironment consists of noise where the energy across thefrequency regions is coherently modulated in time. Bottle-nose dolphins �Tursiops truncatus� have lower maskedthresholds in temporally fluctuating comodulated noise thanin Gaussian noise with the same spectral density level �Bran-stetter and Finneran, 2008�. Thus the thresholds found in thepresent study were probably not being masked by the back-ground noise in the pool.

The 0.125–0.5 kHz signals were only tested under windforce conditions below 2 Beaufort, because more prestimulusresponses occurred at higher wind speeds. This was probablybecause the animals reacted to elements of background noisewhich resembled the test signals. Still, the prestimulus re-sponse rate was generally highest for frequencies below1 kHz. Most transient background noise signals, which maywell trigger prestimulus responses, are in this part of thespectrum. Because both seals were tested within the samesessions, any differences between the thresholds obtained forthe two animals must have been due to differences in theirhearing sensitivity and/or individual differences in their re-sponse criteria, motivational state, or behavior. Differencescould not have been caused by differences in equipment,equipment settings, methodology, personnel, or backgroundnoise. Any changes �increase or decrease� in wind force in-fluencing the background noise level during the 30 min inwhich the two seals were tested will probably have balancedeach other over the very high number of sessions on which

eviation �SD�, and total number of reversal pairs ofe tones �0.125–0.25 kHz� and 13 narrowband FMbased on the number of prestimulus responses in allre the CRs used to calculate the theoretical detection

l 01 Harbor seal 02

s�

Prestimulusresponse

rate�%�

TotalNo. of

reversalpairs

Mean 50%detectionthreshold

�SPL in dBre 1 �Pa, rms�

�SD

Prestimulusresponse

rate�%�

9 124 74�4 96 90 73�4 1011 96 69�5 711 90 64�5 126 103 56�4 75 98 57�5 95 113 55�4 7

10 105 58�4 39 109 63�4 78 109 58�4 38 124 63�4 5

13 103 60�4 85 117 70�4 68 100 106�5 55 106 119�4 35 120 125�4 4

ard dpur

e rateown a

or sea

50%ctionholdin dBa, rm

SD

�4�4�4�4�4�4�5�4�4�4�4�4�3�3�4�4

the thresholds were based.


Did the use of FM signals instead of pure tones influ-ence the hearing thresholds found in the present study? Inmost previous studies of pinniped hearing, except in twoexperiments, pure tones were used as stimuli. Only the hear-ing of a Pacific walrus �Odobenus rosmarus divergens� andtwo Steller sea lions �Eumetopias jubatus� have been testedwith narrowband FM tonal signals �Kastelein et al., 2002,2005� to create a more stable received SPL. In humans, FMsignals tend to have a slightly higher arousal effect than puretones, and therefore slightly lower hearing thresholds��5 dB depending on center frequency and modulation fre-quency; Morgan et al., 1979�. However, the use of FM sig-nals instead of pure tones probably had little effect on thethresholds found in the present study. This assumption isbased on a hearing test with 0.25 kHz signals on a Pacificwalrus �Kastelein et al., 2002�. In that study no differencewas found between thresholds derived with narrowband FMsignals �exactly like those used in the present study; fre-quency modulation only 1% of the center frequency� andthose derived with pure tone signals.

B. Comparison with previous hearing studies inharbor seals

Comparing the hearing of the study seals with that of theother four harbor seals of which the underwater hearing sen-sitivities have been studied is not straightforward. In thevarious studies there are differences in the calibration meth-odology and threshold calculation, and variation in thethreshold data between sessions. Also the background noisemeasurements are often limited, and lower frequency thresh-olds are not always free from masking influences. Research-ers have used various methods and stimulus parameters suchas signal type �pure tone versus FM signal� and signal dura-tion �50–500 ms versus 900 ms�. Also the SPL calculationmethod is not specified for all the studies �peak-to-peak orrms, causing a 9 dB difference�. Despite these complications,general comparisons can be made between the underwateraudiograms of the harbor seals in the present study and thosein previous studies �Møhl, 1968; Terhune, 1988, 1989; Turn-bull and Terhune, 1993, 1994; Terhune and Turnbull, 1995;Kastak and Schusterman, 1998; Southall et al., 2005�. Above4 kHz, the thresholds found in the previous hearing studiesand those found in the present study are similar. However,below 4 kHz the thresholds found in the present study wereup to 20 dB lower than those found in the previous studies.Differences between the hearing sensitivity of the animals inthe present studies and those in previous studies below4 kHz may occur because of the following.

�1� Low-frequency signals were masked by backgroundnoise in previous studies.

�2� Animals in previous studies may have had temporaryhearing loss due to the high background noise levelsfrom pumps before the hearing tests were conducted.

�3� The signal duration in most previous studies was shorterthan the one used in the present study, possibly causingan increase in the hearing threshold �not necessarily be-
cause of the integration time, but probably because it is

difficult for the animals to distinguish between transientsignals in the background noise and the test signals�.

�4� There may have been individual, gender, health condi-tion, or age-related differences in hearing sensitivity be-tween the test animals.

Based on the small minimum audible angles for lowfrequencies, Bodson et al. �2007� concluded that harbor sealsare low-frequency hearing specialists. The present studyshows that harbor seals have a very wide frequency range ofbest hearing, and in quiet conditions are able to hear lowerfrequencies better than previously thought.

C. Ecological significance

The most important finding of this study is that harborseal hearing is more sensitive below 4 kHz than found inprevious studies �Fig. 3�c��. The hearing range of harborseals overlaps in frequency with the loudest and most com-mon anthropogenic noise sources. The effect of anthropo-genic noise on marine mammals is highly variable in typeand magnitude �Severinsen, 1990; Cosens and Dueck, 1993;Richardson et al., 1995�, and harbor seals show avoidancebehavior to certain sounds in certain contexts �Kastelein etal., 2006a, 2006b�. Anthropogenic noise might reduce thetime harbor seals forage in particular areas, thus reducingtheir physiological condition and their reproductive success.In addition to the hearing sensitivity of the harbor seal, theradii of avoidance and disturbance zones around soundsources depend on several other factors such as the generalbackground noise level, water depth, ocean floor sedimentproperties, and the spectrum, source level, and duration ofthe anthropogenic noise. In general, based on the findings ofthe present study, under unmasked conditions, many anthro-pogenic noise sources are audible at greater ranges than for-merly believed. When ambient noise levels in nature arehigher than those of our testing facility, the auditory thresh-olds will be masked, however.

The dominant energy of harbor seal underwater soundproduction is below 2 kHz �Van Parijs and Kovacs, 2002�.The low detection thresholds in this frequency range foundin the present study means that under unmasked conditions,harbor seals can communicate with each other underwaterover greater ranges than formerly believed.

ACKNOWLEDGMENTS

We thank students Aniek van den Berg, Krista Krijgerand Tess van der Drift, and Alejandra Vargas, and volunteersMenno van den Berg, Jesse Dijkhuizen, Petra van der Marel,and Sofie Vandermaele for their help with training the sealsand collecting the data, and Rob Triesscheijn for making thefigures. We thank Dick de Haan �Wageningen IMARES, theNetherlands� for his technical assistance and Veenhuis Medi-cal Audio �Marco Veenhuis and Herman Walstra� for donat-ing the audiometer. We thank Bert Meijering �director ofTopsy Baits, Wilhelminadorp, the Netherlands� for providingspace for SEAMARCO’s Institute, and Hein Hermans forproviding technical support to run the facility. We also thank
Charles Greene �Greenridge Sciences, USA�, Nancy Jen-

nings �Dotmoth.co.uk, Bristol, UK�, and two anonymous re-viewers for their valuable constructive comments on thismanuscript. This study was conducted by SEAMARCO sub-contracted to IMARES �contacts Han Lindeboom andReinier Hille Ris Lambers�. The study was funded byWe@Sea, Noordzee Wind EIA �wind generator parks at sea�,and RIKZ Middelburg, The Netherlands �contacts BelindaKater and Martine van den Heuvel-Greve; acoustic distur-bance of harbor seals in the Westerscheldt�. We thank direc-tor Just van den Broek and curator of animals Henk Brugge�both from Ecomare, Texel� for making the harbor sealsavailable for this project. The seals’ training and testing wereconducted under authorization of the Netherlands Ministry ofAgriculture, Nature and Food Quality, Department of NatureManagement, with Endangered Species Permit No. FF/75A/2005/048.

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underwater detection of tonal signals between 0.125 and 100 khz by harbor seals (phoca vitulina)

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