Introduction to the special issue on fish bioacoustics: Hearing and sound communicationa).

Fish bioacoustics, or the study of fish hearing, sound production, and acoustic communication, was discussed as early as Aristotle. However, questions about how fishes hear were not really addressed until the early 20th century. Work on fish bioacoustics grew after World War II and considerably in the 21st century since investigators, regulators, and others realized that anthropogenic (human-generated sounds), which had primarily been of interest to workers on marine mammals, was likely to have a major impact on fishes (as well as on aquatic invertebrates). Moreover, passive acoustic monitoring of fishes, recording fish sounds in the field, has blossomed as a noninvasive technique for sampling abundance, distribution, and reproduction of various sonic fishes. The field is vital since fishes and aquatic invertebrates make up a major portion of the protein eaten by a signification portion of humans. To help better understand fish bioacoustics and engage it with issues of anthropogenic sound, this special issue of The Journal of the Acoustical Society of America (JASA) brings together papers that explore the breadth of the topic, from a historical perspective to the latest findings on the impact of anthropogenic sounds on fishes.

Sound and sturgeon: Bioacoustics and anthropogenic sounda).

Sturgeons are basal bony fishes, most species of which are considered threatened and/or endangered. Like all fishes, sturgeons use hearing to learn about their environment and perhaps communicate with conspecifics, as in mating. Thus, anything that impacts the ability of sturgeon to hear biologically important sounds could impact fitness and survival of individuals and populations. There is growing concern that the sounds produced by human activities (anthropogenic sound), such as from shipping, commercial barge navigation on rivers, offshore windfarms, and oil and gas exploration, could impact hearing by aquatic organisms. Thus, it is critical to understand how sturgeon hear, what they hear, and how they use sound. Such data are needed to set regulatory criteria for anthropogenic sound to protect these animals. However, very little is known about sturgeon behavioral responses to sound and their use of sound. To help understand the issues related to sturgeon and anthropogenic sound, this review first examines what is known about sturgeon bioacoustics. It then considers the potential effects of anthropogenic sound on sturgeon and, finally identifies areas of research that could substantially improve knowledge of sturgeon bioacoustics and effects of anthropogenic sound. Filling these gaps will help regulators establish appropriate protection for sturgeon.

The career and research contributions of Richard R. Fay.

For over 50 years, Richard R. (Dick) Fay made major contributions to our understanding of vertebrate hearing. Much of Dick's work focused on hearing in fishes and, particularly, goldfish, as well as a few other species, in a substantial body of work on sound localization mechanisms. However, Dick's focus was always on using his studies to try and understand bigger issues of vertebrate hearing and its evolution. This article is slightly adapted from an article that Dick wrote in 2010 on the closure of the Parmly Hearing Institute at Loyola University Chicago. Except for small modifications and minor updates, the words and ideas herein are those of Dick.

Comparison of the saccules and lagenae in six macrourid fishes from different deep-sea habitatsa).

There are substantial interspecific differences in the morphology of the ears of the more than 34 000 living fish species. However, almost nothing is known about the functional significance of these differences. One reason is that most comparative studies have been conducted on shallow-water species with far less focus on the numerous species that inhabit the depths of the oceans. Thus, to get a better sense of ear diversity in fishes and its potential role in hearing, this study focuses on the saccule and lagena, the primary auditory end organs, in six species of the family Macrouridae (rattails), a large group of fishes that typically inhabit depths from 1000 to 4000 m. The inner ears and, particularly, the saccules and lagenae in these species are large with the saccule resembling that of other Gadiformes. The lagenae of all macrourids studied here have serrated edge otoliths and highly diverse hair cell ciliary bundle shapes. The differences found in the inner ear anatomy of macrourids likely reflect the sensory advantages in different habitats that are related to the benefits and constraints at different depths, the fish's particular lifestyle, and the trade-off among different sensory systems.

Marine energy converters: Potential acoustic effects on fishes and aquatic invertebrates.

The potential effects of underwater anthropogenic sound and substrate vibration from offshore renewable energy development on the behavior, fitness, and health of aquatic animals is a continuing concern with increased deployments and installation of these devices. Initial focus of related studies concerned offshore wind. However, over the past decade, marine energy devices, such as a tidal turbines and wave energy converters, have begun to emerge as additional, scalable renewable energy sources. Because marine energy converters (MECs) are not as well-known as other anthropogenic sources of potential disturbance, their general function and what is known about the sounds and substrate vibrations that they produce are introduced. While most previous studies focused on MECs and marine mammals, this paper considers the potential of MECs to cause acoustic disturbances affecting nearshore and tidal fishes and invertebrates. In particular, the focus is on particle motion and substrate vibration from MECs because these effects are the most likely to be detected by these animals. Finally, an analysis of major data gaps in understanding the acoustics of MECs and their potential impacts on fishes and aquatic invertebrates and recommendations for research needed over the next several years to improve understanding of these potential impacts are provided.

Physical effects of sound exposure from underwater explosions on Pacific mackerel (Scomber japonicus): Effects on non-auditory tissues.

Underwater explosions from activities such as construction, demolition, and military activities can damage non-auditory tissues in fishes. To better understand these effects, Pacific mackerel (Scomber japonicus) were placed in mid-depth cages with water depth of approximately 19.5 m and exposed at distances of 21 to 807 m to a single mid-depth detonation of C4 explosive (6.2 kg net explosive weight). Following exposure, potential correlations between blast acoustics and observed physical effects were examined. Primary effects were damage to the swim bladder and kidney that exceeded control levels at ≤333 m from the explosion [peak sound pressure level 226 dB re 1 µPa, sound exposure level (SEL) 196 dB re 1 µPa2 s, pressure impulse 98 Pa s]. A proportion of fish were dead upon retrieval at 26-40 min post exposure in 6 of 12 cages located ≤157 m from the explosion. All fish that died within this period suffered severe injuries, especially swim bladder and kidney rupture. Logistic regression models demonstrated that fish size or mass was not important in determining susceptibility to injury and that peak pressure and SEL were better predictors of injury than was pressure impulse.

Physical effects of sound exposure from underwater explosions on Pacific mackerel (Scomber japonicus): Effects on the inner ear.

Studies of the effects of sounds from underwater explosions on fishes have not included examination of potential effects on the ear. Caged Pacific mackerel (Scomber japonicus) located at seven distances (between approximately 35 and 800 m) from a single detonation of 4.5 kg of C4 explosives were exposed. After fish were recovered from the cages, the sensory epithelia of the saccular region of the inner ears were prepared and then examined microscopically. The number of hair cell (HC) ciliary bundles was counted at ten preselected 2500 µm2 regions. HCs were significantly reduced in fish exposed to the explosion as compared to the controls. The extent of these differences varied by saccular region, with damage greater in the rostral and caudal ends and minimal in the central region. The extent of effect also varied in animals at different distances from the explosion, with damage occurring in fish as far away as 400 m. While extrapolation to other species and other conditions (e.g., depth, explosive size, and distance) must be performed with extreme caution, the effects of explosive sounds should be considered when environmental impacts are estimated for marine projects.

Offshore wind energy development: Research priorities for sound and vibration effects on fishes and aquatic invertebrates.

There are substantial knowledge gaps regarding both the bioacoustics and the responses of animals to sounds associated with pre-construction, construction, and operations of offshore wind (OSW) energy development. A workgroup of the 2020 State of the Science Workshop on Wildlife and Offshore Wind Energy identified studies for the next five years to help stakeholders better understand potential cumulative biological impacts of sound and vibration to fishes and aquatic invertebrates as the OSW industry develops. The workgroup identified seven short-term priorities that include a mix of primary research and coordination efforts. Key research needs include the examination of animal displacement and other behavioral responses to sound, as well as hearing sensitivity studies related to particle motion, substrate vibration, and sound pressure. Other needs include: identification of priority taxa on which to focus research; standardization of methods; development of a long-term highly instrumented field site; and examination of sound mitigation options for fishes and aquatic invertebrates. Effective assessment of potential cumulative impacts of sound and vibration on fishes and aquatic invertebrates is currently precluded by these and other knowledge gaps. However, filling critical gaps in knowledge will improve our understanding of possible sound-related impacts of OSW energy development to populations and ecosystems.

Substrate vibrations and their potential effects upon fishes and invertebrates.

This paper reviews the nature of substrate vibration within aquatic environments where seismic interface waves may travel along the surface of the substrate, generating high levels of particle motion. There are, however, few data on the ambient levels of particle motion close to the seabed and within the substrates of lakes and rivers. Nor is there information on the levels and the characteristics of the particle motion generated by anthropogenic sources in and on the substrate, which may have major effects upon fishes and invertebrates, all of which primarily detect particle motion. We therefore consider how to monitor substrate vibration and describe the information gained from modeling it. Unlike most acoustic modeling, we treat the substrate as a solid. Furthermore, we use a model where the substrate stiffness increases with depth but makes use of a wave that propagates with little or no dispersion. This shows the presence of higher levels of particle motion than those predicted from the acoustic pressures, and we consider the possible effects of substrate vibration upon fishes and invertebrates. We suggest that research is needed to examine the actual nature of substrate vibration and its effects upon aquatic animals.

Sound detection by Atlantic cod: An overview.

The Atlantic cod (Gadus morhua) is among the commercially most important fish species in the world. Since sound plays such an important role in the lives of Atlantic cod and its related species, understanding of their bioacoustics is of great importance. Moreover, since cod are amenable to studies of hearing, especially in open bodies of water, they have the potential to become a "model species" for investigations of fish hearing. To serve as the basis for future studies, and to bring together what is now known about cod hearing, this paper reviews the literature to date. While there is some discussion of other species in the paper, the focus is upon what is already known about cod hearing, and what now needs to be known. An additional focus is on what knowledge of cod hearing tells about hearing in fishes in general.

How to set sound exposure criteria for fishes.

Underwater sounds from human sources can have detrimental effects upon aquatic animals, including fishes. Thus, it is important to establish sound exposure criteria for fishes, setting out those levels of sound from different sources that have detrimental effects upon them, in order to support current and future protective regulations. This paper considers the gaps in information that must be resolved in order to establish reasonable sound exposure criteria for fishes. The vulnerability of fishes is affected by the characteristics of underwater sounds, which must be taken into account when evaluating effects. The effects that need to be considered include death and injuries, physiological effects, and changes in behavior. Strong emphasis in assessing the effects of sounds has been placed upon the hearing abilities of fishes. However, although hearing has to be taken into account, other actual effects also have to be considered. This paper considers the information gaps that must be filled for the development of future guidelines and criteria.

Introduction to the special issue on the effects of sound on aquatic life.

The effects of anthropogenic (man-made) underwater sound on aquatic life have become an important environmental issue. One of the focal ways to present and to share knowledge on the topic has been the international conference on The Effects of Noise on Aquatic Life ("Aquatic Noise"). The conferences have brought together people from diverse interests and backgrounds to share information and ideas directed at understanding and solving the challenges of the potential effects of sound on aquatic life. The papers published here and in a related special issue of Proceedings of Meetings on Acoustics present a good overview of the many topics and ideas covered at the meeting. Indeed, the growth in studies on anthropogenic sound since the first meeting in 2007 reflects the increasing use of oceans, lakes, rivers, and other waterways by humans. However, there are still very substantial knowledge gaps about the effects of sound on all aquatic animals, and these gaps lead to there being a substantial need for a better understanding of the sounds produced by various sources and how these sounds may affect animals.

Physical effects of sound exposure from underwater explosions on Pacific sardines (Sardinops sagax).

Explosions from activities such as construction, demolition, and military activities are increasingly encountered in the underwater soundscape. However, there are few scientifically rigorous data on the effects of underwater explosions on aquatic animals, including fishes. Thus, there is a need for data on potential effects on fishes collected simultaneously with data on the received signal characteristics that result in those effects. To better understand potential physical effects on fishes, Pacific sardines (Sardinops sagax) were placed in cages at mid-depth at distances of 18 to 246 m from a single mid-depth detonation of C4 explosive (4.66 kg net explosive weight). The experimental site was located in the coastal ocean with a consistent depth of approximately 19.5 m. Following exposure, potential correlations between blast acoustics and observed physical effects were examined. Acoustic metrics were calculated as a function of range, including peak pressure, sound exposure level, and integrated pressure over time. Primary effects related to exposure were damage to the swim bladder and kidney. Interestingly, the relative frequency of these two injuries displayed a non-monotonic dependence with range from the explosion in relatively shallow water. A plausible explanation connecting swim bladder expansion with negative pressure as influenced by bottom reflection is proposed.

An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes.

Fishes use a variety of sensory systems to learn about their environments and to communicate. Of the various senses, hearing plays a particularly important role for fishes in providing information, often from great distances, from all around these animals. This information is in all three spatial dimensions, often overcoming the limitations of other senses such as vision, touch, taste and smell. Sound is used for communication between fishes, mating behaviour, the detection of prey and predators, orientation and migration and habitat selection. Thus, anything that interferes with the ability of a fish to detect and respond to biologically relevant sounds can decrease survival and fitness of individuals and populations. Since the onset of the Industrial Revolution, there has been a growing increase in the noise that humans put into the water. These anthropogenic sounds are from a wide range of sources that include shipping, sonars, construction activities (e.g., wind farms, harbours), trawling, dredging and exploration for oil and gas. Anthropogenic sounds may be sufficiently intense to result in death or mortal injury. However, anthropogenic sounds at lower levels may result in temporary hearing impairment, physiological changes including stress effects, changes in behaviour or the masking of biologically important sounds. The intent of this paper is to review the potential effects of anthropogenic sounds upon fishes, the potential consequences for populations and ecosystems and the need to develop sound exposure criteria and relevant regulations. However, assuming that many readers may not have a background in fish bioacoustics, the paper first provides information on underwater acoustics, with a focus on introducing the very important concept of particle motion, the primary acoustic stimulus for all fishes, including elasmobranchs. The paper then provides background material on fish hearing, sound production and acoustic behaviour. This is followed by an overview of what is known about effects of anthropogenic sounds on fishes and considers the current guidelines and criteria being used world-wide to assess potential effects on fishes. Most importantly, the paper provides the most complete summary of the effects of anthropogenic noise on fishes to date. It is also made clear that there are currently so many information gaps that it is almost impossible to reach clear conclusions on the nature and levels of anthropogenic sounds that have potential to cause changes in animal behaviour, or even result in physical harm. Further research is required on the responses of a range of fish species to different sound sources, under different conditions. There is a need both to examine the immediate effects of sound exposure and the longer-term effects, in terms of fitness and likely impacts upon populations.

Directional hearing and sound source localization by fishes.

Directional hearing may enable fishes to seek out prey, avoid predators, find mates, and detect important spatial cues. Early sound localization experiments gave negative results, and it was thought unlikely that fishes utilized the same direction-finding mechanisms as terrestrial vertebrates. However, fishes swim towards underwater sound sources, and some can discriminate between sounds from different directions and distances. The otolith organs of the inner ear detect the particle motion components of sound, acting as vector detectors through the presence of sensory hair cells with differing orientation. However, many questions remain on inner ear functioning. There are problems in understanding the actual mechanisms involved in determining sound direction and distance. Moreover, very little is still known about the ability of fishes to locate sound sources in three-dimensional space. Do fishes swim directly towards a source, or instead "sample" sound levels while moving towards the source? To what extent do fishes utilize other senses and especially vision in locating the source? Further behavioral studies of free-swimming fishes are required to provide better understanding of how fishes might actually locate sound sources. In addition, more experiments are required on the auditory mechanism that fishes may utilize.

The importance of particle motion to fishes and invertebrates.

This paper considers the importance of particle motion to fishes and invertebrates and the steps that need to be taken to improve knowledge of its effects. It is aimed at scientists investigating the impacts of sounds on fishes and invertebrates but it is also relevant to regulators, those preparing environmental impact assessments, and to industries creating underwater sounds. The overall aim of this paper is to ensure that proper attention is paid to particle motion as a stimulus when evaluating the effects of sound upon aquatic life. Directions are suggested for future research and planning that, if implemented, will provide a better scientific basis for dealing with the impact of underwater sounds on marine ecosystems and for regulating those human activities that generate such sounds. The paper includes background material on underwater acoustics, focusing on particle motion; the importance of particle motion to fishes and invertebrates; and sound propagation through both water and the substrate. Consideration is then given to the data gaps that must be filled in order to better understand the interactions between particle motion and aquatic animals. Finally, suggestions are provided on how to increase the understanding of particle motion and its relevance to aquatic animals.

Onset of barotrauma injuries related to number of pile driving strike exposures in hybrid striped bass.

Previous studies exploring injury response to pile driving in fishes presented exposure paradigms (>900 strikes) that emulated circumstances where fish would not leave an area being ensonified. Those studies did not, however, address the question of how many strikes are needed before injuries appear. Thus, the number of strikes paired with a constant single strike sound exposure level (SELss) that can cause injuries is not yet clear. In order to examine this question, hybrid striped bass (white bass Morone chrysops × striped bass Morone saxatilis) were exposed to 8-384 strikes in three different SELss treatments that generated different cumulative sound exposure level values. The treatment with the highest SELss values caused swim bladder injuries in fish exposed to as few as eight pile strikes. These results have important implications for pile driving operations where SELss values meet or exceed the exposure levels used in this study.

It Started in Hawai'i Kai: Reminiscences of 43 Years (and Counting) of Collaboration and Friendship.

This paper discusses the 43+ year collaboration of Arthur Popper and Richard Fay. Over these years, we have co-authored over 30 papers and 55 books. The collaboration benefits from a strong friendship that includes our spouses and children. By any measure, our collaboration must be seen as being successful. The basis for this success is, we think, twofold. First, we have very complementary and overlapping research interests. This has enabled us to tackle issues, whether in research or in planning meetings or books, from different perspectives. Second, a hallmark of our successful collaboration has been our deep and close friendship and the extension of that friendship to our spouses and children. In this paper, we discuss some of the events that have shaped our collaboration, and some of the people who have impacted our lives.

Developing Sound Exposure Criteria for Fishes.

In assessing the impact of aquatic developments, it is important to evaluate whether accompanying underwater sounds might have adverse effects on fishes. Risk assessment can then be used to evaluate new and existing technologies for effective prevention, control, or mitigation of impacts. It is necessary to know the levels of sound that may cause potential harm to different species from different sources as well as those levels that are likely to be of no consequence. The development and use of impact criteria are still at an early stage for fishes.

A Change in the Use of Regulatory Criteria for Assessing Potential Impacts of Sound on Fishes.

The National Marine Fisheries Service (NMFS) currently uses interim criteria developed on the US West Coast to assess the potential onset of peak and cumulative effects of noise on fishes. Analyses performed for this project provided adequate support for the NMFS to use the peak criterion (i.e., area ensonified by 206 dB re 1 µPa peak sound pressure level [SPL(peak)]) for estimating the incidental take of Hudson River sturgeon. Application of the peak criterion (rather than the cumulative criterion) could have implications for future construction projects because estimates of take using SPL(peak) will generally be considerably lower than estimates of take based on the cumulative sound exposure level.