Delphinapterus Leucas) James J

Pure tone audiograms and possible aminoglycoside-induced hearing loss in belugas (Delphinapterus leucas) James J. Finnerana) and Donald A. Carder U.S. Navy Marine Mammal Program, Space and Naval Warfare Systems Center, San Diego, Code 2351, 53560 Hull Street, San Diego, California 92152-5001 Randall Dear Science Applications International Corporation, Maritime Services Division, 3990 Old Town Avenue, Suite 105A, San Diego, California 92110 Traci Belting Point Defiance Zoo and Aquarium, 5400 North Pearl Street, Tacoma, Washington 98466 Jim McBain and Les Dalton Sea World, 500 Sea World Drive, San Diego, California 92109 Sam H. Ridgway U.C. Veterinary Medical Center—San Diego, Department of Pathology, School of Medicine, University of California, La Jolla, California 92093-0612 ͑Received 7 October 2005; revised 10 February 2005; accepted 22 February 2005͒ A behavioral response paradigm was used to measure pure-tone hearing sensitivities in two belugas ͑Delphinapterus leucas͒. Tests were conducted over a 20-month period at the Point Defiance Zoo and Aquarium, in Tacoma, WA. Subjects were two males, aged 8–10 and 9–11 during the course of the study. Subjects were born in an oceanarium and had been housed together for all of their lives. Hearing thresholds were measured using a modified up/down staircase procedure and acoustic response paradigm where subjects were trained to produce audible responses to test tones and to remain quiet otherwise. Test frequencies ranged from approximately 2 to 130 kHz. Best sensitivities ranged from approximately 40 to 50 dB re 1 ␮Pa at 50–80 kHz and 30–35 kHz for the two subjects. Although both subjects possessed traditional ‘‘U-shaped’’ mammalian audiograms, one subject exhibited significant high-frequency hearing loss above 37 kHz compared to previously published data for belugas. Hearing loss in this subject was estimated to approach 90 dB for frequencies above 50 kHz. Similar ages, ancestry, and environmental conditions between subjects, but a history of ototoxic drug administration in only one subject, suggest that the observed hearing loss was a result of the aminoglycoside antibiotic amikacin. ͓DOI: 10.1121/1.1893354͔ PACS numbers: 43.80.Lb ͓WA͔ Pages: 3936–3943 I. INTRODUCTION generally considered the ‘‘standard’’ to which other sensitivity measures ͑e.g., electrophysiological measures͒ are com- The first cetacean audiogram was obtained by Johnson pared ͑e.g., Szymanski et al., 1999͒. ͑1966, 1967͒, who measured pure-tone thresholds in a Behavioral methods are limited, however, by the diffi- trained bottlenose dolphin. Since that time, researchers have culty and costs involved with training marine mammals to investigated hearing sensitivity, frequency selectivity, mask- participate in hearing tests. Most marine mammal psychoa- ing, auditory fatigue, temporal integration, and localization coustic studies have used one or two experimental subjects in dolphins and other marine mammal species ͑review ͑Green et al., 1994͒. Little attention has been given to repli- Nachtigall, 1986; Johnson, 1986; Au, 1993; Nachtigall et al., cating earlier work with additional subjects. The small num- 2000͒. The majority of studies on the auditory capabilities of ber of individuals for whom data are available has resulted in marine mammals have used psychophysical or behavioral lingering questions regarding ‘‘normal’’ hearing for marine response paradigms similar to that employed by Johnson mammal species, typical intraspecific variability, and typical ͑1966, 1967͒. In the behavioral method, the subject is trained hearing loss for different ages and genders. to give a specific response to a particular acoustic stimulus In this paper we report behavioral audiograms for two ͑ ͒ and to withhold the response ͑or provide an alternate re- belugas Delphinapterus leucas . These data augment the sponse͒ in the absence of the stimulus. Behavioral techniques beluga hearing threshold data presented by White et al. ͑ ͒ ͑ ͒ ͑ ͒ allow direct measurements of hearing sensitivity and are 1978 , Awbrey et al. 1988 , Klishin et al. 2000 , and Ridg- way et al. ͑2001͒. Taken together, these data allow estimates to be made of ‘‘normal’’ hearing sensitivity in belugas. The a͒Electronic mail: james.fi[email protected] data from the present study were also unique because they 3936 J. Acoust. Soc. Am. 117 (6), June 2005 0001-4966/2005/117(6)/3936/8/$22.50 revealed significant hearing loss in a subject previously treated with aminoglycoside antibiotics. II. METHODS A. Subjects Test subjects were two male belugas: Beethoven ͑9–11 years old, mass approximately 640 kg͒ and Turner ͑8–10 years, approximately 590 kg͒. Both subjects were born in an oceanarium, had the same father, and had been housed together since shortly after Turner was born. Neither subject had any previous experience with hearing tests or other psychophysical test procedures. The health of the subjects was ascertained through periodic medical examinations by veterinarians. Subjects were healthy during the course of the study, with the exception that from June 2002 until the end of the study Turner was treated off and on for glomerulonephritis as evidenced by periodic hemituria. No ototoxic drugs were used during these periods of treatment. Beethoven required no medical treatment during the study period. Tests were conducted according to a protocol approved by the Institutional Animal Care and Use Committees at the Space and Naval Warfare Systems Center, San Diego and the Point Defiance Zoo and Aquarium. The described experi- ments were conducted in accordance with the Acoustical So- ciety of America’s Guiding Principles in the Care and Use of Animals and followed all applicable U.S. Department of De- fense guidelines. B. Experimental apparatus Figure 1͑a͒ shows the test site located in the ‘‘Rocky Shores’’ beluga habitat at the Point Defiance Zoo and Aquarium, in Tacoma, WA. The exhibit contained approximately 1150 m3 ͑304 000 gal͒ of filtered, ozonated seawater within a large main pool, a shallow connection channel, and an off-exhibit holding pool. The holding pool, which was 9 m in diameter with a depth of 2.7 m, was used to separate the subjects so each could be tested independently. The hearing tests were conducted in the main pool. The main pool was irregularly shaped, roughly 15ϫ20 m, with a surface of sprayed gunite and varying bottom depth and topography. The maximum depth was 4.4 m, sloping up to 1.5 m at the entrance to the channel. The average depth was about 3 m. The main pool volume was 920 m3 ͑243 000 gal͒ and the FIG. 1. ͑a͒ Top-view schematic of the beluga habitat at the Point Defiance 2 Zoo and Aquarium showing the main pool and holding pool. Locations of surface area was 30 m . the test apparatus and trainer positions are marked. Depth contours are ap- The trainer was positioned near a shallow beaching area proximate. ͑b͒ Schematic of the test apparatus with subject positioned on the at the northwest edge of the pool. The test apparatus was biteplate. located along the south side of the pool, near an approximately 10-m-long underwater viewing window built into the themselves on the biteplate, which put their head in a fixed, southwest wall of the pool. A personal computer ͑PC͒, video repeatable position with respect to the sound projector and monitor, and other electronics were housed in a small enclo- receiving hydrophone. Water depth at the apparatus was ap- sure located in the underwater viewing area. proximately 4 m. The depth of the sound projector and sub- The test apparatus ͓Fig. 1͑b͔͒ consisted of a submerged ject was approximately 2 m. The sound projector was posi- polyvinyl chloride ͑PVC͒ frame containing an underwater tioned so that the distance between the projector and the sound projector ͑ITC 10001, ITC 1032, or ITC 1042, de- subject’s ears was approximately 1 m. pending on the test frequency͒, receiving hydrophone ͑B&K Hearing test tones were generated by a multifunction 8105͒, video camera, and a neoprene-covered plastic ‘‘bite- data acquisition board ͑National Instruments PCI-MIO- plate.’’ Subjects were trained to dive underwater and position 16E-1͒ residing within the PC. The generated tones were J. Acoust. Soc. Am., Vol. 117, No. 6, June 2005 Finneran et al.: Beluga audiograms and hearing loss 3937 attenuated ͑HP 355D or TDT PA-5͒, filtered ͑Ithaco 4302͒, was recorded as a ‘‘correct rejection.’’ Tone amplitudes were and amplified ͑BGW PS2͒, before being input to the sound adjusted using a modified up/down staircase procedure ͑e.g., projector: ITC 1001 ͑2–20 kHz͒, ITC 1032 ͑12–50 kHz͒,or Cornsweet, 1962͒: the amplitude was decreased 2 dB after ITC 1042 ͑18–130 kHz͒. Tones were 500 ms in duration, each hit and increased 2 dB after each miss. Hearing thresh- including a 50-ms linear rise and fall time. Sound levels olds for a single session were estimated from the mean sound presented to each subject were calibrated before and after pressure of 10 hit-miss/miss-hit reversal points collected each session, without the subject present, with the receiving within that session. hydrophone located at a position estimated to lie on the sub- The trainer and computer operator monitored the sound ject’s midline at the location of the ears. The hydrophone in the water for any responses by the subject. A small LCD output was amplified ͑B&K 2635͒ and filtered ͑Ithaco 4302͒ was used to display trial parameters ͑e.g., stimulus level, before being digitized by the PCI-MIO-16E-1. During the tone or catch trial, dive time͒ for the trainer. The display was hearing tests the hydrophone was positioned above and in updated just before the start of a trial. The number of trials front of the subject and used to monitor the sound in the per dive was randomized within the following guidelines: water, including the hearing test tones and any sounds pro- Dives were ended only after correct responses.

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