11 Hearing
Arthur N. Popper and Anthony D. Hawkins
CONTENTS
11.3 The Importance of Sound to Fishes Today
11.4 Primer on Underwater Sound
11.4.1 Underwater Sound and Fishes
11.5.2 Response of the Ear to Sound Stimulation
11.7.1 Other Aspects of Hearing by Fishes
11.8 What Don’t We Know about Fish Hearing (Future Directions)?
11.9 Anthropogenic Sound and Fishes
11.1 Introduction
It has been known since the days of Aristotle that fishes make and detect sounds (reviewed in Moulton, 1963). The fish ear was perhaps first described by E. H. Weber (1820) and G. Retzius (1881) (see Figure 11.1 for illustrations from the original publications). However, it was not until the experimental work of G. H. Parker (1903), and then K. von Frisch (1938) (who later went on to win the Nobel Prize for his work on the dance language of bees) and his students (e.g., von Frisch and Stetter, 1932; von Frisch and Dijkgraaf, 1935), that hearing in fishes came to be better understood in terms of sensitivity to different frequencies and overall capabilities.
The following key gives the structures related to hearing. Other structures are associated with the vestibular sense: l: lagena; ms: macula sacculi; o: otolith; rl, rs, ru: rami of eighth cranial nerve to the otolith end organs; s: saccule; u: utricle.
11.2 How and Why Hearing?
Critical questions are when, how, and why did hearing evolve in vertebrates? Hearing evolved in the earliest vertebrates (e.g., Pumphrey, 1950; Van Bergeijk, 1967; Popper et al., 1992; Popper and Fay, 1997). Van Bergeijk (1967), following Pumphrey (1950), proposed that the ear evolved from surface receptors, perhaps ancestral to the lateral line, that dropped below the surface and eventually became covered. Van Bergeijk hypothesized that this provided a system that would not be directly affected by water motion and that, over time, the frequency range of this accelerometer-like system would have served a number of functions, including both auditory and vestibular senses.
But why? Consider that the most primitive vertebrates lived in water. Other senses these animals may have had – light and chemical receptors – had limited ranges over which they could detect stimuli. Vision would be restricted by the light levels and murkiness of the water, and so the “visual field” for the animals was likely measured in centimeters or, perhaps, in meters. Chemical reception is at the mercy of currents and is a very slow way to glean information.
Sound, on the other hand, is less restricted by most environmental conditions, and in water, sound travels very fast and is directional (e.g., Urick, 1983; Rogers and Cox, 1988; also www.dosits.org). Thus, by evolving a system to detect sound, fish ancestors developed a means to get information about predators, prey, and their environment from long distances and very quickly. In other words, the evolution of hearing resulted in fishes sensing the “acoustic scene,” or soundscape, which provided them with a far larger waterscape than any other sense (Popper and Fay, 1997; Fay and Popper, 2000; Fay, 2009).
11.3 The Importance of Sound to Fishes Today
All fishes, including the bony fishes, elasmobranchs, lampreys, and hagfishes, have ears. While we have data on hearing of relatively few species, it is highly likely that all fishes use the soundscapes to glean information important for survival. Even though all fishes hear, a lower number of fishes have been shown to make and use sounds for purposes of reproduction, territorial behavior, and other behaviors (e.g., Hawkins and Myrberg, 1983; Hawkins, 1993; Ladich, 2019).
11.4 Primer on Underwater Sound
In order to understand fish hearing, it is critical to have a basic understanding of underwater sound. A fuller discussion can be found at www.dosits.org and in several recent papers that specifically deal with sound and fishes (Hawkins and Popper, 2018a; Popper and Hawkins, 2018, 2019).
Sound is generated by the vibration of a source and depends upon the elasticity of the medium. As the source vibrates, it imparts energy, which passes on as a propagated wave within which the medium’s particles move back and forth over the same location and do not, themselves, travel. The waves that travel result from the fact that the particles oscillate along the line of transmission, thereby transmitting their oscillatory motion to their neighbors. This particle motion is accompanied by waves that include increases (compression) and reductions (rarefaction) in pressure. Together, the compressions and rarefactions that propagate from the sound source are referred to as the sound pressure.
In air, due to the low density of the medium, particle motion does not travel far from the source, and terrestrial hearing is primarily sound pressure detection. However, in water, which is far denser, particle motion continues to be a significant part of the acoustic environment for considerable distances from the source (Urick, 1983). Indeed, in open water, distant from any boundaries (e.g., surface or bottom), the sound pressure radiated from a simple acoustic source falls off as 1/r, where r is the distance from the source (van Bergeijk, 1964; Ainslie and de Jong, 2016). Far from the source (“far field”), the energies associated with acoustic pressure and acoustic particle velocity are equal, whereas close to the source (“near field”), the particle velocity component of the field contains more energy. The distance of the transition point is related to the nature of the source as well as to the frequency of the signal, with the distance greater for lower frequencies (van Bergeijk, 1964).
It is critical to appreciate that particle motion is inherently directional along its axis of transmission. In essence, particle motion, whether considered in terms of particle displacement, velocity, or acceleration, is a vector quantity. Indeed, if properly constructed, a particle motion detector (based on three mutually perpendicular accelerometers) can detect the axis of sound propagation. Moreover, as will be discussed later, the ears of fishes are ideally “designed” to serve as accelerometers that detect the directional component of the particle motion, thus determining sound source direction.
In contrast, the sound pressure is a scalar quantity and acts in all directions. Thus, a single sound pressure detector cannot determine the axis of propagation of the sound. Several detectors are necessary, spaced well apart, to achieve this.
11.4.1 Underwater Sound and Fishes
It is critical to understand that the inner ear of fishes responds only to particle motion and not to sound pressure (Hawkins and Popper, 2018a; Popper and Hawkins, 2018), although as discussed in Section 11.5.3, some fishes can also detect sound pressure using ancillary structures. The importance of particle motion for fish hearing was recognized decades ago by Dijkgraaf (1960) and others, but with few exceptions, investigators, even to this day, focus on sound pressure as a stimulus in measuring underwater sound, which includes reporting hearing in terms of sound pressure rather than particle motion. While this is somewhat understandable due to the difficulties in measuring particle motion and the complexities of defining sound fields in experimental tanks (Rogers et al., 2016; Popper and Hawkins, 2018), it also means that much of the earlier and even some recent data are difficult, if not impossible, to interpret in terms of detection capabilities or the sound fields to which fish were exposed (Popper and Hawkins, 2018; Popper et al., 2019b). Moreover, this also makes defining the soundscapes detected by fishes in the wild difficult, since most field recordings of sound use hydrophones sensitive to sound pressure, whereas most fish species are only detecting particle motion.
11.5 How Do Fishes Hear?
External auditory structures are not needed by fishes because of the density similarities between the water and the body. Thus, an impinging sound passes right through the body and cannot be detected unless there are structures of different densities with which the sound can interact. Most bony fishes have two such discontinuities. The first are the otoliths of the inner ear (Figures 11.1b and 11.2), which are about three times denser than the rest of the body. The second may be a bubble of gas, such as the swim bladder, that is much less dense, and more compressible, than the water (Figure 11.1a).
(Figure © 2019 Anthony D. Hawkins, all rights reserved.)
11.5.1 The Inner Ear
The inner ear of fishes consists of three semicircular canals for detection of angular motion of the body (Platt, 1983) and three otolith organs, the saccule, lagena, and utricle, that respond to linear acceleration and gravity as well as sound (Figures 11.1b and 11.2). In most bony fishes, the otolith organs contain a single, solid mass of calcium carbonate, the otolith, that grows year by year, creating “rings” that can be used to determine the age of the fish. The shape and orientation of the otolith differ between the three otolith organs in fishes. All other vertebrates, including non-teleost bony fishes, sharks, and terrestrial vertebrates, have similar calcium carbonate material in their otolith organs but in the form of crystals, otoconia, embedded in a gelatinous mass. The functional basis for having an otolith rather than otoconia is as yet unknown (Popper et al., 2005; Schulz-Mirbach et al., 2019).
Each otolith organ has a sensory epithelium (or macula) that is overlain by the otolith (Figure 11.3) (Popper and Hawkins, 2019; Schulz-Mirbach et al., 2019). The sensory epithelium contains sensory hair cells that are very similar to those found in the ears of terrestrial vertebrates (Coffin et al., 2004). The sensory cells are surrounded by supporting cells and are innervated by the eighth cranial nerve (Figure 11.4). They have a ciliary bundle consisting of a single true cilium, the kinocilium, and a series of stereocilia, on their apical ends (e.g., Dale, 1976; Popper and Hoxter, 1981). The otolith overlies the epithelium and is separated from it by a thin otolithic membrane (Figure 11.4) that connects microvilli on the surface of the supporting cells and the rough surface of the otolith itself (e.g., Dunkelberger et al., 1980). While this has never been demonstrated experimentally, the otolithic membrane probably limits the relative motion between the otolith and the epithelium.
(Figure © 2019 Anthony D. Hawkins, all rights reserved.)
(Figure © 2019 Anthony D. Hawkins, all rights reserved.)
Hearing results from the fish’s body moving in the sound field with the water, while the otolith moves with a different amplitude and phase due to its very different density. This relative motion between the otolith and the underlying sensory epithelium results in bending of the ciliary bundles and opening of ion channels in the cilia, which leads to chemical changes in the cells and the release of a neurotransmitter that stimulates the innervating afferent nerve fibers (e.g., Hudspeth and Corey, 1977).
Moreover, the sensory cells are both morphologically and physiologically polarized, so that bending of the bundle in different directions results in different responses from each cell, as shown in Figure 11.5, with maximum response when the stereocilia bend in the direction of the kinocilium (e.g., Flock, 1964). In effect, each sensory cell is a directional detector!
(Figure © 2019 Anthony D. Hawkins, all rights reserved.)
The sensory epithelium contains large numbers of hair cells that continue to be added as a fish grows (e.g., Lombarte and Popper, 1994). Thus, a small fish may have hundreds of hair cells in the saccular epithelium, while a larger fish may have hundreds of thousands. Most importantly, the hair cells are organized into “orientation groups,” as shown in Figure 11.6, where all of the cells in a particular region are oriented in the same general direction.
(Figure © 2019 Arthur N. Popper, all rights reserved.)
11.5.2 Response of the Ear to Sound Stimulation
The otolith organ responds to the particle motion component of the sound field. Since particle motion is directional, sound from a particular direction will maximally stimulate sensory cells oriented in that direction, while cells oriented in other directions will give a different level of response, as shown in Figure 11.5.
Considering that each fish has six otolith organs, each oriented on a somewhat different plane, and that even within one organ the cells may be oriented in different directions (e.g., see the orientation on the utricles in Figure 11.6), it is clear that fishes have sensory cells that will give maximum response to signals from any direction (Figure 11.7). Once this information from sensory cells oriented in different directions is combined in the central auditory system, fishes can derive the direction of a sound source with some accuracy (reviewed in Walton et al., 2017; Hawkins and Popper, 2018a; Schulz-Mirbach et al., 2019). At the same time, as pointed out by Schuijf and his colleagues, information from just particle motion is the same from opposite directions, and they proposed that some fishes may additionally use sound pressure to resolve this 180 degree ambiguity (e.g., Schuijf, 1975; Schuijf and Hawkins, 1983).
(Unpublished data from Hawkins and King. Figure © 2019 Anthony D. Hawkins, all rights reserved.)
The response is most clearly seen in Figure 11.7, which shows the directional sensitivity of a single neuron in the anterior saccular branch of the left auditory nerve of the Atlantic cod, Gadus morhua, obtained using a shaking table to apply particle velocity stimuli from different directions in three orthogonal planes at 125 Hz. The radial axis is the level of nerve response.
The level of response shown in the graphs reflects the direction in which the nerve showed maximum output, suggesting that the hair cells had maximum response from that direction (e.g., Figure 11.5). This is particularly seen as the two peaks in the directional responses within each plane, separated by 180 degrees. Thus, in the top two graphs, maximum response was when stimulation was from anterior to posterior (along the axis of the fish), while there was minimal response to stimulation from right and left. This result is as expected, since the nerve branch that was recorded primarily innervates hair cells oriented anteriorly and posteriorly (Figure 11.6). At the same time, when the fish was turned sideways in the lower graph, there were no sensory cells in the anterior region of the saccule oriented in that direction, and so there is minimal response. If, however, the recording had been done from the nerve innervating the utricle, there would have been cells oriented to the side (see Figure 11.5).
11.5.3 Ancillary Structures
By being a particle motion detector, the fish ear can only detect a limited frequency range, and sensitivity to sounds at any particular frequency is also limited. At the same time, some fishes can detect a wider frequency bandwidth and have better sensitivity than others, and this is accomplished by adding the detection of sound pressure, as occurs in species that hear above about 500 Hz (Figure 11.8). However, in order to detect sound pressure, fishes needed ancillary structures that are responsive to pressure changes. In all cases, such a structure is a bubble of gas, most often in the form of the swim bladder.
Species and data sources: (a) Common dab (Limanda limanda) (Chapman and Sand, 1974); Atlantic salmon (Salmo salar) (Hawkins and Johnstone, 1978); Atlantic cod (Gadus morhua) (Chapman and Hawkins, 1973); herring (Clupea harengus) (Enger, 1967). (b) European perch (Perca fluviatilus) (Wolff, 1967); blue-striped grunt (Haemulon sciurus) (Tavolga and Wodinsky, 1965); damselfish (Eupomacentrus partitus) (Myrberg Jr and Spires, 1980); squirrelfish (Adioryx xantherythrus) (Coombs and Popper, 1979); goldfish (Carassius auratus) (Jacobs and Tavolga, 1967); soldierfish (Myripritis kuntee) (Coombs and Popper, 1979.)(Figures ©2019 Anthony D. Hawkins, all rights reserved.)
The swim bladder’s role in hearing is simple. When the gas is subject to compression and rarefaction by a sound wave, the walls of the chamber move, and this serves as a secondary sound source that reradiates the energy as both sound pressure and particle motion. This particle motion has the potential to stimulate the inner ear.
However, for the reradiated particle motion to stimulate the ear, it must not attenuate as it propagates from the air chamber to the ear (Alexander, 1966). Presumably, the degree of attenuation depends on the distance between the air bubble and the ear, and the nature of intervening tissues such as bones and muscle, although this has never been investigated. At the same time, it is clear, as will be discussed in Section 11.7 on hearing capabilities, that fishes with close proximity between the gas bubble and the ear, as in the Atlantic cod (Gadus morhua), or where there is some direct link between the gas bubble and the inner ear, as in the goldfish (Carassius auratus) and the soldier fish (Myripristis berndti), hear a wider range of frequencies and show higher sensitivity than do fishes in which the gas bubble and inner ear are further apart, such as salmonids (Figure 11.8) (hearing data reviewed in Ladich and Fay, 2013).
Fishes with direct links between the inner ear and an air bubble appear to hear better than all other species, since the movements of the swim bladder caused by sound pressure are directly tied to the ear. The best-known example of this connection is found in the otophysan fishes (goldfish, catfishes, etc.), where a series of bones, the Weberian ossicles, connect the swim bladder to the ear (Figures 11.1a and 11.9) (Weber, 1820), so that the motion of the walls of the swim bladder are carried directly to the fluids of the inner ear (Poggendorf, 1952; Alexander, 1964) in a manner analogous to the function of the mammalian middle ear bones.
(Figure © 2019 Anthony D. Hawkins, all rights reserved.)
Outside of the otophysans, many other species, from diverse taxonomic families, have evolved specialized connections that bring the swim bladder into close, or intimate, proximity to the inner ear. These include, but are not limited to, swim bladder extensions that terminate on the walls of the saccule, as in the soldierfish (Coombs and Popper, 1979), swim bladder extensions that are within the ear, as in the clupeid fishes (O’Connell, 1955), or gas bubbles that are totally unconnected to the swim bladder and actually make up one wall of the saccule, as in the mormyrids (McCormick and Popper, 1984).
11.6 Diversity of Fish Ears
A perusal of Retzius (1881) and more recent work (e.g., Deng et al., 2013) shows remarkable diversity in the morphology of the ears of fishes. While this diversity leads to obvious questions about the functional significance of different ears, we actually know very little about the relationship between form and function. Indeed, this is an area open to considerable speculation (e.g., Hawkins and Popper, 2018a; Popper and Hawkins, 2018; Schulz-Mirbach et al., 2019).
The diversity is seen in several distinct ways. First, there is a wide range in the size and shape of the otolith organs themselves, and particularly of the saccule, the main hearing end organ (Figure 11.1b). Second, there is substantial diversity in the size, shape, and overall structure of the otoliths in different species, and particularly in the saccular otolith (Figures 11.1a and 11.2) (e.g., Popper et al., 2005; Lychakov et al., 2006). And finally, there is wide variation in the hair cell orientation patterns on the saccules (and to a lesser degree the lagena and utricles) of different species (Figure 11.6). And this does not include the diversity in other aspects of the inner ear, such as the lengths of ciliary bundles on hair cells in different epithelial regions (and in different species) (e.g., Platt and Popper, 1984) and potentially, variation in the nature of the connection between the epithelium and the otolith (the otolith membrane).
Unfortunately, we still have very little functional data on the inner ears of fishes (Popper and Hawkins, 2018; Schulz-Mirbach et al., 2019). Thus, we do not know whether the diversity in structure relates to differences in the way sounds are processed in the ear in different species, but with all structures giving the same information, or whether the different structures suggest that different species are extracting different information from the sounds.
11.7 What Do Fishses Hear?
There is great diversity in hearing capabilities among various species (Figure 11.8). At the same time, the majority of studies to date (reviewed in Ladich and Fay, 2013) must be treated with caution for several reasons (Popper et al., 2019b). First, hearing data were most often determined in terms of detection of sound pressure, whereas, as discussed earlier, particle motion is the predominant hearing stimulus for most species.
Second, most earlier work has been done in tanks, the vast majority of which have significant acoustic problems (e.g., Duncan et al., 2016; Rogers et al., 2016). A third problem with studies is that hearing was studied using physiological methodologies that only give hearing in terms of what the ear can detect, as opposed to behavioral studies in which the responses depend not only on what is detected by the ear but also on analysis by the central nervous system (Sisneros et al., 2016; Popper and Hawkins, 2019). Thus, while physiological methods give some sense of the hearing range of fishes as well as some indication of sensitivity at each frequency, results from behavioral studies are of far greater value.
Despite these issues, it is possible to develop some understanding of what fishes can hear (Figure 11.8). It is, for example, clear that all fishes studied to date (perhaps 100 species) can hear, and that the hearing range extends from below 50 Hz to perhaps 10–30 Hz, or even lower in some species (Sand and Karlsen, 2000), and up to 300–500 Hz. Moreover, species that detect sound pressure may hear up to approximately 1000 Hz, while fishes with some of the aforementioned specializations can detect sounds to 3–4 kHz.
Measurement of the lowest levels of sound that fishes can detect at any particular frequency is problematic since results vary even for the same species when determined in different laboratories, as shown for the goldfish (Ladich and Fay, 2013; Popper et al., 2019b), and with the method of determination. Moreover, studies may have calibrated sound levels in terms of sound pressure when the fish was actually responding to some unknown level of particle motion.
Perhaps the most useful data are from studies where hearing has been determined under well-defined acoustic conditions, either in open bodies of water or in very specialized tanks that allow careful sound calibration of both pressure and particle motion. Such data are shown in Figure 11.8a for studies done in the open sea. In this figure, the common dab (and the Atlantic salmon) are only sensitive to particle motion, and so they only have a relatively narrow bandwidth of hearing, whereas species in which the gas-filled swim bladder is close to the ear, such as the Atlantic cod, also detect sound pressure, and so they have an increased hearing bandwidth. Finally, the Atlantic herring has the widest bandwidth because of the presence of an air bubble within the ear cavity. Many other species have been tested in various types of chambers (Figure 11.8b) and must be viewed with a number of caveats (Section 11.4.1) (reviewed in Popper et al., 2019b). Despite these caveats, however, these data show the range of hearing capabilities of different species, depending on factors such as connections between the swim bladder and the ear. In particular, goldfish and soldierfish have connections between the swim bladder and the inner ear and so hear to over 3 kHz. In contrast, the closely related squirrelfish does not have connections to the ear, so it is unlikely to be stimulated by the swim bladder and therefore, has a narrower hearing range.
11.7.1 Other Aspects of Hearing by Fishes
While hearing sensitivity and sound detection are important, it is more important that the auditory system of fishes extract far more information about a sound than just its presence. Indeed, for sound to be useful, animals must be able to discriminate between sounds to know “friend from foe,” to determine the direction of a sound source so that the fish can move towards or away from the signal, and to detect a biologically relevant signal in the presence of other ambient noises that make up every acoustic environment (e.g., sound from waves, other biological sources, and wind).
While there are as yet few studies on sound detection capabilities of fishes, it is clear that at least the species studied (and likely all species) are capable of signal analysis that provides a good deal of information about sounds detected, including discrimination of sounds that are close to one another in frequency and intensity (reviewed in Fay and Megela Simmons, 1999), and determining the direction of a sound source (reviewed in Hawkins and Popper, 2018a). And, while studies on topics other than threshold determination have mainly been done on a single species, the goldfish, it is likely that fishes have far more complex sound processing capabilities, which are similar to those of terrestrial vertebrates, including mammals.
One other critically important capability is detection of a biologically relevant signal in the presence of background noise. Indeed, hearing in normal environments always occurs in the presence of background noise. If that background noise is below the hearing sensitivity of a fish, it has no impact on hearing. However, if the background (ambient) noise is higher, it may be above the hearing sensitivity of the fish and thus, as shown in Figure 11.8, increase the lowest detectable sound level for the species. This means that the lowest sound levels detectable by fishes that hear well, such as Atlantic cod and Atlantic herring, are limited by their ability to detect and discriminate biologically important sounds in the presence of the ambient noise background. In such conditions, the level of noise limits the lowest sound level that an animal can detect. Interference in detection of biologically relevant sounds by other sounds (including natural or human-made sound) is referred to as masking (Fay and Megela Simmons, 1999).
11.8 What Don’t we Know about Fish Hearing (Future Directions)?
While we know a reasonable amount about fish hearing capabilities and mechanisms, it is also clear that we know far less about hearing by fishes than we do for other vertebrate taxa. This was dealt with in papers that focused on the major unanswered questions about fish hearing (Hawkins et al., 2015; Hawkins and Popper, 2016). This list for further study related to fishes is extensive but includes, among other things:
- The functional significance of diversity in ear structure, otolith shape, hair cell orientation patterns, length of ciliary bundles on hair cells, etc. Do these reflect different species extracting different information from sounds detected or different evolutionary approaches to doing the same acoustic tasks?
- The function of the ear itself and the interactions between sound, the otoliths, and the sensory epithelia – including hair cells oriented in different directions.
- Mechanisms of central processing of sounds in the brain and the role of the brain in extracting signals from noise, sound direction, etc.
- The specific function and role of the swim bladder and other ancillary structures that, presumably, enhance hearing capabilities. Are they, for example, frequency specific? How do their roles change with fish depth?
- Hearing capabilities of a more diverse group of fishes, with particular emphasis on detection and processing of particle motion. This includes determination of particle motion thresholds as well as developing a better understanding of processing of complex sounds.
- While not discussed in this chapter, there are many questions on the acoustic behavior of fishes in the wild, including how fishes use their soundscape. There are also questions on how fishes actually use sound for communication.
11.9 Anthropogenic Sound and Fishes
There is a growing concern about the potential effects of anthropogenic (human-made) sound on fishes as well as other aquatic life. The sources of such sounds are quite diverse and range from sounds of vessels, to sounds used in exploration for off-shore oil and gas, to sounds resulting from the construction of wind farms. Importantly, as the number and variety of anthropogenic sounds increase, they have the potential to have a broad impact on aquatic life that ranges from death, to physiological effects such as increased stress levels, to loss of hearing sensitivity to behavioral changes – all of which can potentially cause significant impacts on fitness (Popper and Hawkins, 2016; Hawkins and Popper, 2018b; Harding et al., 2019; Hawkins et al., 2020).
While there is concern about a wide range of potential effects, perhaps two are most important, since they can happen as long as fishes are located near enough to an anthropogenic sound that it can be heard or that the sound can interfere with hearing (masking).
The first of these are related to behavioral changes that result from fishes changing patterns of behavior, such as migratory routes, feeding sites, or breeding sites (to name just a few). Behavioral changes in fishes exposed to anthropogenic sounds have been shown in a number of cases with wild animals, and in each case the behavioral changes could have a broad impact on the daily activities of animals (e.g., Engås et al., 1996; Hawkins et al., 2014).
The second, though related, major effect is when the presence of anthropogenic sound masks the ability of fishes to detect biologically relevant sounds such as those produced by conspecifics or those produced by predators or prey. Thus, the results of masking mean that the “communication distance” over which a fish can detect a sound of relevance decreases, thereby reducing fitness (Dooling and Leek, 2018; Popper and Hawkins, 2019).
In effect, concerns about potential effects of anthropogenic sounds on fishes becomes a “driving force” for studies of fish hearing today. This is because it is imperative to know much more about hearing and acoustic behavior if we are to understand potential effects of different sounds and sound levels on fishes and make efforts to either mitigate these sounds, if they are too loud, or develop regulatory actions that will protect fish from harm while still allowing human activities in the water. These and other issues regarding potential impacts of anthropogenic sound have been reviewed a number of times recently (e.g., Popper et al., 2014; Andersson et al., 2017; Carroll et al., 2017; Popper and Hawkins, 2019; Popper et al., 2019a; Putland et al., 2019).
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