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Hearing in Fishes Under Noise Conditions

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Hearing in Fishes Under Noise Conditions JARO 6: 28–36 (2005) DOI: 10.1007/s10162-004-4043-4 Hearing in Fishes under Noise Conditions LIDIA EVA WYSOCKI AND FRIEDRICH LADICH Institute of Zoology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria Received: 13 October 2003; Accepted: 27 September 2004; Online publication: 3 December 2004 ABSTRACT hearing specialists, are limited by noise regimes in their environment. Ourcurrentknowledgeon sound detection in fishes is Keywords: auditory evoked potential, auditory mainly based on data acquired under quiet laborato- sensitivity, hearing specializations, masking, teleosts ry conditions. However, it is important to relate auditory thresholds to background noise in order to determine the signal-detecting abilities of animals in the natural environment. We investigated the influ- ence of two noise levels within the naturally occurring INTRODUCTION range on the auditory sensitivity of two hearing specialists (otophysines) and a hearing generalist. The auditory system is particularly important for Audiograms of the goldfish Carassius auratus, the aquatic vertebrates when visual orientation is restrict- lined Raphael catfish Platydoras costatus and the ed. Sounds from different sources provide them with pumpkinseed sunfish Lepomis gibbosus (hearing gen- information relevant for survival, e.g., finding mates eralist) were determined between 200 and 4000 Hz and prey or avoiding predators. The natural environ- (100Y800 Hz for L. gibbosus) under laboratory con- ment of fishes, especially that of marine fishes ditions and under continuous white noise by record- (Knudsen et al. 1948; Wenz 1962; Urick 1983; ing auditory evoked potentials (AEPs). Baseline Myrberg 1990), but also freshwater habitats (Hawkins thresholds showed greatest hearing sensitivity around and Johnstone 1978; Rogers and Cox 1988; Lugli 500 Hz in goldfish and catfish and at 100 Hz in the and Fine 2003), is characterized by a permanent sunfish. Continuous white noise of 110 dB RMS background noise of abiotic (currents, rain, seismic elevated the thresholds by 15Y20 dB in C. auratus events, coastal surf) and biotic (vocalizations of ani- and by 4Y22 dB in P. costatus. White noise of 130 dB mals, photosynthesis) origin. In addition, the amount RMS elevated overall hearing thresholds significantly of man-made noise caused by ship and air traffic, in the otophysines by 23Y44 dB. In the goldfish, hydroelectric power plants, or drilling is increasing. threshold did not shift at 4 kHz. In contrast, auditory Thus noise is an omnipresent environmental con- thresholds in the sunfish declined only at the higher straint on the auditory system of fishes and ultimately noise level by 7Y11 dB. Our data show that the AEP determines the detectability of sounds relevant to recording technique is suitable for studying masking their orientation toward prey, predators, and con- in fishes, and that the occurrence and degree of the specifics, and to acoustic communication in their threshold shift (masking) depend on the hearing environment. sensitivity of fishes, the frequency, and noise levels Most investigations on sound detection in fishes, tested. The results indicate that acoustic communi- however, were performed under quiet laboratory con- cation and orientation of fishes, in particular of ditions, and their results may be ill-suited to informa- tion on the ability of fishes to detect signals in their natural environment. In terrestrial animals it is long known (e.g., Fletcher 1940) that the detection of one Present address: Lidia Eva Wysocki, Department of Biology, Univer- signal can be impaired by the presence of another (i.e., sity of Maryland, College Park, MD 20742, USA. noise), a phenomenon termed masking. Several prior Correspondence to: Lidia Eva Wysocki & Department of Biology & University of Maryland & College Park, MD 20742, USA. Telephone: investigations have addressed this issue in fishes. (431)-4277-54515; fax: (431)-4277-9544; email: [email protected] Tavolga (1967) and Buerkle (1968, 1969) observed 28 WYSOCKI AND LADICH: Hearing in Fishes under Noise 29 elevated auditory thresholds in the presence of which are available from prior studies (Fay 1974; Fay increased background noise in the squirrelfish Hol- and Coombs 1983). All animals were kept in planted ocentrus rufus, the grunt Haemulon sciurus, and the cod aquaria whose bottoms were covered with sand, Gadus morhua. Studies conducted in the field on equipped with half flower pots as hiding places, filtered several other marine teleosts (Melanogrammus aeglefi- by external filters, and maintained at a 12L:12D cycle. nus, Pollachius pollachius, G. morhua, Molva molva; The fishes were fed live Tubifex sp., chironomid larvae, Chapman 1973; Chapman and Hawkins 1973) have or commercially prepared flake food (Tetramin\) confirmed that masking can occur even under daily. No submerged filters or air stones were used in relatively quiet sea conditions, suggesting that abso- order to reduce noise in the holding tanks. Back- lute sensitivity of the auditory system is less important ground noise in the holding tanks ranged from 110 to than the ability to discriminate between relevant 115 dB LLeq for the otophysines, and from 124 to 127 sound stimuli and background noise. All those dB LLeq for L. gibbosus. All experiments were per- experiments together pointed out the need to relate formed with the permission of the Austrian Commis- auditory thresholds to background noise in order to sion on Experiments in Animals (GZ 68.210/50-Pr/4/ determine the signal-detecting abilities in the natural 2002). environment. The main objectives of our study were to investi- Auditory evoked potential recordings gate (1) to which extent white noise at naturally occurring sound pressure levels (SPL) affect hearing The AEP recording protocol used in this study thresholds, (2) to which degree different frequen- followed that recently described in Wysocki and cies are masked, and (3) whether fishes with dif- Ladich (2001, 2002, 2003). Therefore, only a brief ferent hearing abilities are differently affected by summary of the basic technique is given here. similar noise levels. A further goal (4) was to eval- During the experiments, the fishes were mildly uate the usefulness of the auditory evoked potential immobilized with Flaxedil (gallamine triethiodide; (AEP) method in studying masking in fishes by com- Sigma). The dosage used was 0.90Y1.9 mggj1 for paring our results to behaviorally obtained data (Fay C. auratus,1.3Y3.3 mggj1 for P. costatus, and 2.4Y5.8 1974; Fay and Coombs 1983) in goldfish. This is a first mggj1 for L. gibbosus. This dosage allowed the fishes step before addressing a wider range of issues related to retain slight opercular movements during the to the impacts of natural noise on the biology of experiments but without significant myogenic noise fishes. to interfere with the recording. Test subjects were Our test animals were two hearing specialists, the secured in a bowl-shaped plastic tub (diameter: 37 cypriniform Carassius auratus (goldfish) and the cm, water depth: 8 cm, 2 cm layer of fine sand) lined sound-producing siluriform Platydoras costatus (lined on the inside with acoustically absorbent material Raphael catfish), and a vocal hearing generalist, the (air-filled packing wrap) in order to reduce resonan- perciform Lepomis gibbosus (pumpkinseed sunfish). ces and reflections (for the illustration of the effect, Noise is highly variable in the natural environment see Fig. 1 in Wysocki and Ladich 2002). Fishes were (Wenz 1962; Hawkins and Johnstone 1978; Urick 1983) and its biological relevance mostly unknown. Therefore and in order to compare our results to previous data, we applied white (Gaussian) noise with a relatively flat frequency spectrum as a masker. MATERIALS AND METHODS Animals Test subjects were seven goldfish C. auratus (88Y 98 mm standard length, 22.3Y28 g body weight) from a pond near Vienna, six lined Raphael catfish P. cos- tatus (99Y124 mm standard length; 22.9Y38.8 g body mass), and seven pumpkinseed sunfish L. gibbosus (79Y94 mm; 15.6Y26.2 g). The latter two species were FIG. 1. Cepstrum-smoothed (coefficients: 64) spectra of mean obtained from local pet suppliers. Goldfish were cho- laboratory noise (lower line), white noise of 110 dB LLeq (mid line) and of 130 dB LLeq (upper line). Cepstrum-smoothed spectra are sen because there exists a large amount of behavioral plotted for better representation. Cepstrum smoothing is a mathe- and neurophysiological data on diverse aspects of matical calculation (Noll 1967) for the representation of the mean their hearing abilities including behavioral masking energy content of fluctuating sound spectra. 30 WYSOCKI AND LADICH: Hearing in Fishes under Noise positioned below the water surface (except for the con- sure levels of tone-burst stimuli were reduced in 4 dB tacting points of the electrodes, which were maximally steps until the AEP waveform was no longer apparent. 1 mm above the surface) in the center of the plastic The lowest SPL for which a repeatable AEP trace could tub. be obtained, as determined by overlaying replicate A respiration pipette was inserted into the subject’s traces, was considered the threshold (Kenyon et al. mouth. Respiration was achieved through a simple 1998). temperature-controlled (24 T 1 -C), gravity-fed water A hydrophone (Bru¨el & K jaer 8101, frequency circulation system. The AEPs were recorded by using range: 1 HzY80 kHz T 2 dB; voltage sensitivity: j184 silver wire electrodes (0.25 mm diameter) pressed re 1 V/mPa) was placed close to the right side of the firmly against the skin. The portion of the head above animals (2 cm apart) in order to determine absolute the water surface was covered by a small piece of SPLs underwater in close vicinity of the subjects. Kimwipes tissue paper to keep it moist and to ensure Control measurements showed that, in accordance proper contact during experiments. The recording with theoretical expectations (due to increasing electrode was placed in the midline of the skull over distance from the loudspeaker), SPLs decreased with the region of the medulla and the reference electrode increasing distance from the center of the tub as well cranially between the nares.
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