[MARMAM] Abstracts - Aquatic Mammals (2007) - Special issue on hearing

Dagmar Fertl dfertl at geo-marine.com
Fri May 18 21:26:39 PDT 2007

Apologies in advance, to those of you on both listserves who will receive cross-postings. The following are the contents and abstracts for the most recent issue of Aquatic Mammals. This journal was established by the European Association for Aquatic Mammals (EAAM) in 1974. The EAAM and the Board of the Alliance of Marine Mammal Parks and Aquariums sponsor the journal. 


Aquatic Mammals accepts a wide variety of papers on the care, conservation, medicine, and science of marine mammals.  Dr. Jeanette Thomas of Western Illinois University is the editor and Dr. Kathleen Dudzinski of Mystic Aquarium is the co-editor. These abstracts are posted as a courtesy to the Marmam editors and the sponsoring societies, as well as the managing editor of Aquatic Mammals.


The latest issue of Aquatic Mammals is a special issue entitled: Electrophysiological Measurements of Hearing in Marine Mammals. The issue is divided into six parts: review, bottlenose dolphin, harbor porpoise, Pacific white-sided dolphin, new techniques, and pinnipeds, with a foreword by Michel André and Paul Nachtigall, the organizers of this special issue. 


The special issue is available on CD, as well as a limited number of hard copies. See the journal’s Web site for more details at: http://www.aquaticmammalsjournal.org <http://www.aquaticmammalsjournal.org/> . 


Please find below, the addresses (including email) of the authors to whom reprint requests and other inquiries should be directed. Thank you for your continued interest in these postings, as well as other publication postings to the listserves.


With regards,


Dagmar Fertl

Geo-Marine, Inc.

dfertl at geo-marine.com

 <http://www.geo-marine.com/> http://www.geo-marine.com



André, M.*, and P.E. Nachtigall. 2007. Electrophysiological measurements of hearing in marine mammals. Aquatic Mammals 33(1):1-5.


*LAB, Laboratori d’Applicacions Bioacústiciques, Universitat Politècnica de Catalunya, Rambla Exposició s/n, 08800 Vilanova I la Geltrú, Barcelona, Spain. Direct author correspondence to : M. André at - Email:  <mailto:Michel.Andre at upc.edu> Michel.Andre at upc.edu


No abstract was provided, what follows is a summary. 


In March 2006, an international workshop was organized by Michel André and Paul Nachtigall and hosted by the European Cetacean Society during its 20th Conference in Gdynia Poland. The workshop brought together experts in the field of bioacoustics and hearing. The experts presented a summary of the ‘state-of-the-art’ of AEP studies on cetaceans and non-cetacean species as well as provided directions for future research. This special issue represents the output of the workshop. The article then briefly discusses the content of each article in the issue. 


Nachtigall, P.E., T.A. Mooney, K.A. Taylor, and M.M.L. Yuen. 2007. Hearing and auditory evoked potential methods applied to odontocete cetaceans. Aquatic Mammals 33(1):6-13.


*Marine Mammal Research Program, Hawaii Institute of Marine Biology, University of Hawaii, P.O. Box 1106, Kailua, HI 96734, USA. Email:  <mailto:nachtiga at hawaii.edu> nachtiga at hawaii.edu


Auditory evoked potential (AEP) procedures have been increasingly used to measure hearing processes in aquatic mammals. They have been demonstrated to be useful in measuring the audiograms of stranded animals like infant sperm whales (Physeter macrocephalus) and Risso’s dolphins (Grampus griseus). Modulation rate transfer functions (MRTF) demonstrating appropriate stimulus presentation rates are usually measured prior to recording audiograms with odontocetes. Measures comparing behavioral and AEP audiograms with the same animals have generally shown good correspondence between data gathered using the two procedures. AEPs and acoustic brainstem responses (ABRs) also have been used to measure hearing while an animal is actively echolocating. This technique of measuring the animal’s ability to hear its own outgoing signals, as well as the returning echoes, allows experimenters to develop a new understanding of the processes underlying echolocation.


Supin, A.Ya.* and V.V. Popov. 2007. Improved techniques of evoked-potential audiometry in odontocetes. Aquatic Mammals 33(1):14-23.


*Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninksy Prospect, 119071 Moscow, Russia. Email:  <mailto:alex_supin at sevin.ru> alex_supin at sevin.ru


Efficiency of the auditory evoked-potential (AEP) method of audiometry in odontocetes can be markedly increased by the use of (1) stimulus parameters providing maximal AEP amplitude and (2) methods of better extraction of AEP from background noise. A train of short tone pips is a very effective stimulus that allows using the same analysis technique as the sinusoidally amplitude-modulated (SAM) stimulus, but provides much higher AEP amplitude. For AEP extraction from background noise, apart from a commonly used averaging method (mean-based extraction), mean-based extraction is very effective when the noise is not stationary and includes short, but big spikes or bursts.



Popov, V.V.*, A.Ya. Supin, M.G. Pletenko, M.B. Tarakanov, V.O. Klishin, T.N. Bulgakova, and E.I. Rosanova. 2007. Audiogram variability in normal bottlenose dolphins (Tursiops truncatus). Aquatic Mammals 33(1):24-33.


Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninksy Prospect, 119071 Moscow, Russia. Email:  <mailto:popov_vl at sevin.ru> popov_vl at sevin.ru


In odontocetes, underwater audiograms have been obtained mostly in one or two individuals in a species. A representative number of animals should be investigated to document variability. In the present study, an attempt has been made to estimate the audiogram mean and scatter among normal bottlenose dolphins (Tursiops truncatus). Measurements were made in dolphins captured in the wild and kept in captivity for three to five months, using auditory evoked potential (AEP) technique (envelope-following response [EFR]) to measure underwater hearing thresholds. Fourteen subjects, 11 males and 3 females, provisionally from 3 to 15 years old, were investigated. Hearing thresholds were measured at frequencies from 8 to 152 kHz with ¼-octave steps. All the subjects had qualitatively similar audiograms, except one. The averaged audiogram featured the best sensitivity (the threshold below 50 dB re 1 μPa) at 45 kHz. Thresholds rose slowly to lower frequencies (up to 65 dB at 8 kHz) and steeply at higher frequencies (up to 97 dB at 152 kHz). Inter-individual standard deviations varied, depending on frequency, from 4.4 to 11.7 dB, mostly not more than 10 dB. One animal featured a significant hearing loss with increased thresholds at frequencies above 54 kHz. An analytical formula for a standard audiogram is suggested based on these data. 



Hernandez, E.N.*, S. Kuczaj, D.S. Houser, and J.J. Finneran. 2007. Middle- and long-latency auditory evoked potentials in bottlenose dolphins (Tursiops truncatus) resulting from frequent and oddball stimuli. Aquatic Mammals 33(1):34-42.


*Department of Psychology, Box 5025, The University of Southern Mississippi, 118 College Drive, Hattiesburg, MS 39406, USA. Email:  <mailto:erica.hernandez at yahoo.com> erica.hernandez at yahoo.com


Middle- and long-latency auditory evoked potentials 9AEP) have not been extensively studied in marine mammals. Differences in longer latency potentials resulting from infrequent “oddball” stimuli inserted within a train of repeated, or “standard,” auditory stimuli can potentially be used to detect the discrimination ability of an individual. To investigate the characteristics of evoked responses resulting from the oddball paradigm, AEPs were recorded using 100-ms pure tones as stimuli and recording AEP epochs of 500 ms from two bottlenose dolphins (Tursiops truncatus). The P50 response to a 40-kHz pure tone was attenuated when that stimulus was repeated (the standard stimulus), with an 80% probability of occurrence. When a 30-kHz oddball tone was presented (20% probability of occurrence), however, the P50 response amplitude increased, indicating dishabituation to the novel stimulus. The attenuation of the P50 response to the standard tone was observed when the standard and oddball tones were reversed (30-kHz standard; 40-kHz oddball). The results demonstrated sensory gating, either habituating to a repeated stimulus (“gating out”) and/or dishabituating to a novel stimulus (“gating in”). The presence of one or both of these responses suggests that the P50 response to oddball stimuli has the potential to indicate discrimination of a particular set of auditory stimuli.


Finneran, J.J.*, D.S. Houser, and C.E. Schlundt. 2007. Objective detection of bottlenose dolphin (Tursiops truncatus) steady-state auditory evoked potentials in response to AM/FM tones. Aquatic Mammals 33(1):43-54.


*U.S. Navy Marine Mammal Program, Space and Naval Warfare Systems Center, San Diego, CA 92152, USA. Email:  <mailto:james.finneran at navy.mil> james.finneran at navy.mil


Auditory steady-state responses were measured in a bottlenose dolphin (Tursiops truncatus) and used to illustrative objective techniques to determine the presence and absence of a response. Experimental measurements were conducted under water in a quiet pool. Sound stimuli were pure tones that were both amplitude and frequency modulated. Evoked responses were recorded using noninvasive surface electrodes. Two frequency-domain techniques were used to assess the presence or absence of a response. The F test compares the evoked potential power at a single frequency (the amplitude modulation frequency) to the noise power averaged over adjacent frequencies. Magnitude-squared coherence (MSC) is a ratio of the signal power at a single frequency to the signal-plus-noise power and reflects the degree to which the system output is determined by the input. For the measurements here, both techniques provided identical results. Evoked potential thresholds based on the lowest detected response compared favorably to behavioral thresholds obtained in the same environment.


Lucke, K.*, P.A. Lepper, B. Hoeve, E. Everaarts, N. van Elk, and U. Siebert. 2007. Perception of low-frequency acoustic signals by a harbour porpoise (Phocoena phocoena) in the presence of simulated offshore wind turbine noise. Aquatic Mammals 33(1):55-68.


*FTZ Westkueste, Christian-Albrechts-Universitaet zu Kiel, Buesum, Germany. Email:  <mailto:lucke at ftz-west.uni-kiel.de> lucke at ftz-west.uni-kiel.de


Using auditory evoked potential (AEP) methods, a study was conducted on a harbour porpoise (Phocoena phocoena) at the Dolfinarium Harderwijk in The Netherlands. The study measured the audible range of wind turbine sounds and their potential masking of wind turbine sounds and their potential masking effects on the acoustic perception of the animal. AEPs were evoked with two types of acoustic stimuli: (1) click-type signals and (2) amplitude-modulated signals. The masking noise resembling the underwater sound emissions of an operational wind turbine was simulated. At first, the animal’s hearing threshold was measured at frequencies between 0.7 and 16 kHz. Subsequently, these measurements were repeated at frequencies between 0.7 and 2.8 kHz in the presence of two different levels of masking noise. The resulting data show a masking effect of the simulated wind turbine sound at 128 dB re 1 μPa at 0.7, 1.0, and 2.0 kHz. This masking effect varied between 4.8 and 7.3 dB at those frequencies. No significant masking was measured at a masking level of 115 dB re 1 μPa. The available data indicate that the potential masking effect would be limited to short ranges in the open sea, but limitations exist to this conclusion and all estimates are based on existing turbine types, not taking into account future developments of larger and potentially noisier turbine types.


Beedholm, K.*, and L.A. Miller. 2007. Automatic gain control in harbor porpoises (Phocoena phocoena)? Central versus peripheral mechanisms. Aquatic Mammals 33(1):69-75.


*Institute of Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark. Email:  <mailto:beedholm at mail.dk> beedholm at mail.dk


A previous study indicated no automatic gain control (AGC) in the auditory system of a harbor porpoise (Phocoena phocoena) as revealed by recording auditory evoked potentials to simulated echoes (Beedholm et al., 2006). The same harbor porpoise did change the rate and amplitude of its echolocation clicks during stationary echolocation when presented with an artificial target at a fixed delay. The animal spontaneously changed its click rate in such a way that emitted level (in dB, arbitrary reference) of a click decreased as the inter-click interval (ICI) decreased (click emission rate increases), according to a 14.5 log (ICI) function. The same relationship was found when the animal swam toward a target (a fish). It reduced the amplitude of its clicks as it approached the target with a -14 to -17 log r (best-fit), which is close to the expected -20 log r found in other studies. The combined results indicate an incomplete AGC working on the transmitter side and might be explained by constraints in the sound production apparatus that couple the sound amplitude to the click rate.


Au, W.W.L.*, J.A. Thomas, and K.T. Ramirez.  2007. Characteristics of the auditory brainstem evoked potential of a Pacific white-sided dolphin (Lagenorhynchus obliquidens).  Aquatic Mammals 33(1):76-84.


*Marine Mammal Research Program, Hawaii Institute of Marine Biology, University of Hawaii, P.O. Box 1106, Kailua, HI 96734, USA. Email:  <mailto:wau at hawaii.edu> wau at hawaii.edu


Auditory brainstem responses (ABRs) of a Pacific white-sided dolphin (Lagenorhynchus obliquidens) in the presence of masking noise were measured at John G. Shedd Aquarium in Chicago. The dolphin was trained to wear suction cups with 1-cm diameter, gold-plated metallic electrodes typically used for human EEG measurements embedded in the cups. The animal was trained to station in a hoop, facing a sound projector 5 m away. ABR thresholds were obtained by progressively reducing the level of click stimuli, having peak frequencies of 8, 16, 32, 64, 80, and 100 kHz. The thresholds were obtained in the presence of broadband masking noise. The ABR waveforms were slightly different than for other odontocetes, having 7 to 8 waves present – the most for any odontocetes measured so far. The response latency of 1.3 to 1.5 ms is similar to those of other dolphins of approximately the same size. The peaks in the Fourier transform of the ABR waveform occurred at 650 and 1,200 Hz, very similar to the 600 to 650 and 1,100 to 1,200 Hz for Tursiops truncatus. The deepest null in the spectrum, which occurred at about 950 Hz, was much deeper than for the bottlenose dolphin. Masked ABR thresholds expressed in peak-to-peak values were between 38 and 56 dB above the rms values of the masking noise.



Delory, E., J. del Rio, J. Castell, M. van der Schaar, and M. André. 2007. OdiSEA: An autonomous portable auditory screening unit for rapid assessment of hearing in cetaceans. Aquatic Mammals 33(1):85-92.


*LAB, Laboratori d’Applicacions Bioacústiciques, Universitat Politècnica de Catalunya, Rambla Exposició s/n, 08800 Vilanova I la Geltrú, Barcelona, Spain. Direct author correspondence to : M. André at - Email:  <mailto:Michel.Andre at upc.edu> Michel.Andre at upc.edu


The screening of marine mammals’ auditory capabilities is a vital and delicate diagnosis elaboration process. A self-configurable, compact, and portable battery-operated screening tool is now available, named OdiSEA, which enables the collection of species-related auditory characteristics and a rapid diagnosis of hearing impairment, both in controlled and field situations such as rehabilitation facilities and at stranding sites, respectively. Acoustic stimulation is achieved with a calibrated piezoelectric ceramic that transduces sound either through a gel-filled suction cup or, more conventionally, from a few meters distance to the subject in a pool. System portability and the integration of a wideband (>150 kHz) auditory brainstem response (ABR) and multiple auditory steady-state response (multiple ASSR) evoked potentials system shortens diagnosis times significantly for both simple auditory tests and more detailed screening of auditory function. This unit should simplify and significantly accelerate the collection of audiograms in cetaceans.


Taylor, K.A.*, P.E. Nachtigall, T.A. Mooney, A.Ya. Supin, and M.L. Yuen. 2007. A portable system for the evaluation of marine mammals’ auditory capabilities. Aquatic Mammals 33(1):93-99.


*Marine Mammal Research Program, Hawaii Institute of Marine Biology, University of Hawaii, P.O. Box 1106, Kailua, HI 96734, USA. Email:  <mailto:kristent at hawaii.edu> kristent at hawaii.edu


We have created a portable system that is capable of measuring the hearing thresholds of marine mammals. It was designed for the purpose of testing the auditory capabilities for a wide range of marine mammal individuals and species. This system consists of multiple individual components, independently purchased or assembled. The major component of the system is a standard laptop computer with custom software that is able to both generate outgoing signals and acquire the corresponding brain measurements in response to those outgoing signals. The system has been, and still is, in an ongoing state of improvement and optimization with the goal of having a final system that could be used in nearly all field conditions.


André, M.*, E. Delory, E. Degollada, J-M Alonos, J. del Rio, M. van Der Schaar, J.V. Castell, and M. Morell. 2007. Identifying cetacean hearing impairment at stranding sites. Aquatic Mammals 33(1):100-109.


*LAB, Laboratori d’Applicacions Bioacústiciques, Universitat Politècnica de Catalunya, Rambla Exposició s/n, 08800 Vilanova I la Geltrú, Barcelona, Spain. Email:  <mailto:Michel.Andre at upc.edu> Michel.Andre at upc.edu


While noise is now considered a marine hazard that can directly affect cetaceans and induce a stranding, no clinical approach has yet introduced that detection of a possible hearing loss at a stranding site as a necessary practice. This can be explained by the lack of time when facing vital decisions for the animal’s welfare as well as the unavailability of reliable, lightweight, autonomous, and portable audiometry equipment. Herein, we correlate measured electrophysiological evidence of a permanent threshold shift (PTS) in a rehabilitated striped dolphin (Stenella coeruleoalba) that prevented its release, with the postmortem analysis of an abnormal dilation of the central nervous system ventricles that prevented the correct acoustic reception of the animal. We further propose to follow a five-minute auditory evoked potential (AEP) standard protocol of hearing measurements in-air on cetaceans at a stranding site that includes the stimulation of auditory brainstem responses (ABRs) with a single 4-μs broadband (>150 kHz) pulse at three decreasing levels (129, 117, and 105 dBpp re 1 μPa at 15 cm), which covers most of the cetaceans’ known maximum acoustic sensitivity and allow the immediate sensing of an individual’s hearing capability before any final clinical decision is taken.

Houser, D.S.*, D.E. Crocker, C. Kastak, J. Mulsow, and J.J. Finneran. 2007. Auditory evoked potentials in northern elephant seals (Mirounga angustirostris). Aquatic Mammals 33(1):110-121.


*BIOMEMETICA, 7951 Shantung Drive, Santee, CA 92071-3432, USA. Email:  <mailto:biomimetica at cox.net> biomimetica at cox.net


Auditory evoked potentials (AEPs) were investigated in northern elephant seals (Mirounga angustirostris) to characterize the responses elicitied by different acoustic stimulus types, examine temporal resolving capabilities, and evaluate the potential for using evoked responses to estimate hearing sensitivity. Clicks and tone pips were presented to individual seals to characterized evoked responses to broad- and narrowband stimuli. Tone pip trains and sinusoidally amplitude-modulated (SAM) tones were used to determine modulation rate transfer functions (MRTF) of the auditory system and to determine if the magnitude of the envelope-following response (EFR) relative to stimulus level can be used to estimate hearing thresholds. Click evoked responses were characterized by three early positive peaks (app. 2.6, 4.4, and 6.1 ms) and a dominant negative peak at 7.2 ms and had average amplitudes of 264 nV (peak-to-peak [pk-pk]) for a corresponding stimulus level of 126 dB re 20 μPa (pk-pk). The use of dissociative drugs for the immobilization of the seals showed no demonstrable effect on the latencies or amplitudes of the click evoked response. Both the rate following response (RFR) and EFR amplitudes were maximal when the stimulus repetition rate or the amplitude modulation rate, respectively, were <100 Hz. EFR amplitudes at the rate of amplitude modulation tracked near linearly with stimulus level. Thresholds for a 4-kHz, SAM tone were estimated to be 45 dB re 20 μPa. Thus, the recording of AEPs is a viable means of studying auditory processes in the northern elephant seal.


Mulsow, J.* and C. Reichmuth. 2007. Electrophysiological assessment of temporal resolution in pinnipeds. Aquatic Mammals 33(1):122-131.


*Department of Ocean Sciences, Earth and Marine Sciences Building, University of California-Santa Cruz, Santa Cruz, CA 95060, USA. Email:  <mailto:jmulsow at ucsc.edu> jmulsow at ucsc.edu


Studies of auditory temporal processing in marine mammals have traditionally focused on the highly refined temporal capabilities of dolphins and other odontocete cetaceans. However, a recent electrophysiological investigation of manatee (Trichechus manatus) hearing has shown their temporal resolution to be better than expected, leading to speculation that enhanced temporal processing capabilities are adaptive for underwater sound localization. This study measured evoked responses from several California sea lions (Zalophus californianus), a harbor seal (Phoca vitulina), and a northern elephant seal (Mirounga angustirostris) to determine how well the auditory systems of these amphibious mammals resolve rhythmic stimuli. Trains of broadband clicks were presented in air at repetition rates from 125 to 1,500 s-1, and the averaged evoked responses elicited by those stimuli were recorded from the skin. Rate-following responses were detected in the sea lions at rates up to 1,000 s-1, with an upper limit of temporal resolution estimated at 875 to 1,000 s-1. This upper limit is better than previously anticipated and was further substantiated by limited testing with the harbor seal and northern elephant seal. While these findings might support an underwater sound localization hypothesis, measurements comparable to those of the pinnipeds were also obtained in a phylogenetically similar terrestrial mammal: a domestic dog (Canis familaris). It is therefore possible that increased temporal resolution in pinnipeds and other non-echolocating marine mammals is not a result of the evolutionary pressure of an aquatic environment.


Reichmuth, C.*, J. Mulsow, J.J. Finneran, D.S. Houser, and A.Ya. Supin. 2007. Measurement and response characteristics of auditory brainstem responses in pinnipeds. Aquatic Mammals 33(1):132-150.


*Institute of Marine Sciences, Long Marine Laboratory, 100 Shaffer Road, University of California-Santa Cruz, Santa Cruz, CA 95060, USA. Email:  <mailto:coll at ucsc.edu> coll at ucsc.edu


The measurement of auditory evoked potentials (AEPs) has proven to be a useful tool for examining the auditory physiology of odontocete cetaceans and there is growing interest in applying this electrophysiological approach to study the hearing of other marine mammals. The aim of the current investigation was to examine some of the basic measurement and response characteristics of the auditory brainstem response (ABR) in pinnipeds. The subjects were California sea lions (Zalophus californianus), harbor seals (Phoca vitulina), and northern elephant seals (Mirounga angustirostris) there were awake, sedated, or anesthetized during in-air testing. Auditory stimuli were broadband clicks and Hanning-gated tone bursts there were presented binaurally in a direct field. The amplitude and waveform of the ABRs were evaluated as a function of subject sate, electrode type and position, analog bandpass filtering, stimulus presentation rate, and stimulus bandwidth. Results indicate that the ABRs were of highest amplitude when measured from subdermal electrodes arranged in a common reference configuration, with the cephalic electrode placed 2 to 4 cm forward of the ears on the dorsal midline of the head. The ABR waveforms were generally similar among the species tested, although the amplitude of the elephant seal ABR was much smaller than that of the other two species at similar stimulus levels. Bandpass filtering of the ABR resulted in improved signal-to-noise ratios but also caused reduction in response amplitude and distortion of the ABR waveform at high-pass settings above 65 Hz. Five-cycle tone bursts provided the best tradeoff between response amplitude and frequency specificity. The amplitude of ABRs evoked by clicks and tone bursts as a function of stimulus level was approximately linear for California sea lions and harbor seals over a range of app. 25 dB. Visually estimated thresholds for California sea lions were noise limited but were sensitive enough to show hearing loss in one older subject. These findings should inform future research efforts involving electrophysiological assessment of auditory function, hearing sensitivity, and noise i

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