The effects of noise on the auditory sensitivity of the bluegill sunfish, Lepomis macrochirus

Abstract

As concerns about the effects of underwater anthropogenic noises on the auditory function of organisms increases, it is imperative to assess if all organisms are equally affected by the same noise source. Consequently, auditory capabilities of an organism need to be evaluated and compared interspecifically. Teleost fishes provide excellent models to examine these issues due to their diversity of hearing capabilities. Broadly, fishes can be categorized as hearing specialists (broad hearing frequency range with low auditory thresholds) or hearing generalists (narrower frequency range with higher auditory thresholds). The goal of this study was to examine the immediate effects of white noise exposure (0.3–2.0 kHz, 142 dB re: 1 μPa) and recovery after exposure (1–6 days) on a hearing generalist fish, bluegill sunfish (Lepomis macrochirus). Noise exposure resulted in only a slight, but not statistically significant, elevation in auditory threshold compared to fish not exposed to noise. In combination with results from our previous studies examining effects of noise on a hearing specialist fish, the fathead minnow (Pimephales promelas), this study provides evidence supporting the hypothesis that fish's auditory thresholds can be differentially affected by noise exposure.

Introduction

Recently, there has been heightened concern about the effects of underwater noise on freshwater and marine organisms. This is a result of the increasing amount of noise in the underwater acoustic environment associated with anthropogenic sources (Richardson et al., 1995; Gordon and Moscrop, 1996). Though sounds generated from boats and ships are considered the main sources, there are a vast number of anthropogenic noise sources, including underwater explosions, sonars, air guns, dredges, ocean science studies, hydroelectric dams, fishing equipment with acoustic deterrent devices, and noises associated with oil and gas production (Richardson et al., 1995; Richardson and Würsig, 1997). Though most of these sources generate noise only as a by-product, many produce it intentionally. Regardless, there are an expansive number of potential noise sources an aquatic or marine organism may encounter in its environment.

Despite the amount of noise in the underwater environment, there have been few studies directly addressing the auditory effects of noise on aquatic organisms. Many behavioral studies have been conducted, but they may not give a comprehensive picture of the effects of noise exposure on the physiology of the auditory system. For example, Myrberg (1990) reported that many fish species have been found in the vicinity of offshore petroleum drilling platforms, which are considered quite noisy. He brings forth a pertinent question to consider: are the fishes assembled in this area because they are deafened and their ability to acoustically assess their surroundings is severely compromised or does the noise simply not affect their auditory system? Furthermore, fishes, as well as marine mammals, may react differently to noises, either by fleeing the area, remaining stationary, or even become attracted to the noise source (Richardson and Würsig, 1997). Richardson and Würsig (1997) remark that because an organism may endure noise exposure does not necessarily mean that the noise itself does not have any adverse effects.

In addition, it is erroneous to think that all organisms would be equally affected by a noise source. This has already been demonstrated by examining behavioral effects of noise on marine mammals in terms of sex, age, general activity, time of year, and habitat (Richardson and Würsig, 1997). Though, one factor that is often neglected is the organism's general hearing ability. Different organisms have variation in their auditory capabilities, in terms of not only hearing frequency ranges but also auditory threshold levels. It can, therefore, be hypothesized that hearing ability also plays an important role in the response an organism has to a noise source. The end result is that there are multitudes of different noise sources in the underwater environment along with an abundance of different organisms that can potentially be affected, and very little information so far addressing the effects of noise on hearing thresholds of species with different auditory capacities.

The first step in addressing these issues is finding appropriate animal models, and fishes provide a means of better understanding the effects of noise on hearing. What makes fish such suitable models, is that there is no one universal ‘fish ear’ due to the vast amount of structural and physiological diversity among the inner ear and its peripheral structures, which causes great degrees of differences in hearing abilities among fishes (Platt and Popper, 1981, Schellart and Popper, 1992, Popper and Fay, 1993, Popper and Fay, 1999). Therefore, fishes offer the unique opportunity to examine a variety of hearing mechanisms and their responses to noise exposure.

Essentially, a fish's sensitivity to sound depends on the presence of a gasbladder (von Frisch, 1938, Coombs and Popper, 1979, Yan et al., 2000) or gas-holding auditory ancillary structures: suprabranchial chambers (Schneider, 1941, Ladich and Yan, 1998, Yan, 1998), otic gasbladders (von Frisch, 1938, Stipetic, 1939, Yan and Curtsinger, 2000, Fletcher and Crawford, 2001), otic bullae (Blaxter et al., 1979, Denton et al., 1979, Gray and Denton, 1979; Blaxter et al., 1981) and the degree of coupling or proximity these structures have with the fish's inner ear. One common type of accessory structure is the Weberian apparatus, of otophysan fishes (i.e. minnows and catfish), which are modified vertebrae connecting the anterior portion of the gasbladder to the inner ear (Evans, 1925). This accessory apparatus acts to transduce the pressure component of sound, associated with the vibration of the gasbladder, into particle motion which directly stimulates the sensory epithelium of the inner ear (Finneran and Hastings, 2000). Fishes with direct coupling devices or auditory ancillary structures are referred to as hearing specialists because they hear over a wide frequency range with lower auditory threshold. Conversely, fishes without these coupling devices and that hear over a narrower frequency range with higher auditory thresholds are referred to as hearing generalists (Tavolga and Wodinsky, 1963, Popper and Fay, 1993, Popper and Fay, 1999). Consequently, along with the anatomical diversity associated with the fish's auditory structures, there is a correlation with anatomy and hearing capabilities (see review in Platt and Popper, 1981). Therefore, it has been speculated that noise may not affect every fish equally due to the diversity of the fish ear itself (Hastings et al., 1996).

There have been several previous studies examining the physical effects and morphological damage associated with intense noise exposure on the inner ear of fishes (Enger 1981; Hastings, 1995; Hastings et al., 1996). Two of the species examined were hearing generalists, the oscar (Astronotus ocellatus) and cod (Gadus morhua), though the cod has wider hearing range than most hearing generalist species (Sand and Karlsen, 1986; Astrup and Møhl, 1993, Astrup and Møhl, 1998), while one was a hearing specialist, the goldfish (Carassius auratus). All the studies detected mechanical injury to the sensory hair cells after exposure to intense sound ranging from 180 to 204 dB (re: 1 μPa), but damage was limited in the oscar (A. ocellatus) compared to that seen in the goldfish (C. auratus). Hastings et al. (1996) attributed this difference in hair cell damage to variation in overall hearing ability (hearing generalists vs. specialists) between the two species. All of these studies only addressed morphological effects of noise exposure, not auditory threshold effects.

Studies examining auditory effects of noise on fishes, have been limited and have, so far only examined hearing specialist fishes. Popper and Clarke (1976) investigated the effects of pure tone noise stimuli (149 dB, re: 1 μPa) on the goldfish. Our previous study (Scholik and Yan, 2001), examined the effects of white noise on auditory sensitivity of the fathead minnow (Pimephales promelas) and indicated that the effects of intense white noise exposure (142 dB, re: 1 μPa) was frequency and exposure duration dependent. The next issue of interest was to examine if white noise exposure yielded similar results in a fish without enhanced hearing mechanisms, a hearing generalist fish.

The purpose of this study was to examine how intense noise affected the auditory sensitivity of a hearing generalist fish, the bluegill sunfish (Lepomis macrochirus). The bluegill sunfish (Family Centrarchidae) is considered a relatively important sport fish in the North America. Its natural habitats ranges from southern Canada to northern Mexico, including the midwest and eastern regions of the USA (Trautman, 1981; Helfman et al., 1997). Due to its wide range of distribution in various types of aquatic habitats, the bluegill has the potential to be exposed to a variety of acoustic environments. Hence, it is a useful model for the present study.

We hypothesized that since hearing generalists, like bluegill sunfish, lack Weberian ossicles or ancillary structures to enhance hearing sensitivity, and thus have an auditory range that is narrower in frequency bandwidth with higher overall auditory thresholds than hearing specialists (e.g. fathead minnows) (Scholik and Yan, 2001, Scholik and Yan, 2002), their hearing thresholds should be less affected by noise. Specifically, the two main objectives of our study were to (1) examine the immediate effects of noise exposure (0.3–2.0 kHz, 142 dB re: 1 μPa) using various exposure duration (2, 4, 8 and 24 h), and to (2) assess recovery (1–6 days) of auditory thresholds after exposure to 24 h of white noise using the auditory brainstem response (ABR) recording technique. In addition, we were interested in comparing the results from the present study, for a hearing generalist, to those we previously obtained (Scholik and Yan, 2001) for a hearing specialist fish. This comparison allows us to investigate if the impacts of noise exposure can be equally applied to fishes of different hearing abilities.