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.

The importance of underwater sounds to gadoid fishes.

The codfish family includes more than 500 species that vary greatly in their abundance in areas like the North Sea and are widely fished. Gadoids (codfish) gather at particular locations to spawn, where they exhibit complex reproductive behavior with visual and acoustic displays. Calls have been described from seven species, including the Atlantic cod and haddock. They vocalize by means of a specialized apparatus, consisting of rapidly contracting striated muscles (the drumming muscles) attached to the gas-filled swim bladder. Several gadoids, such as the ling and the Greenland cod, possess drumming muscles and are likely to make sounds. Non-vocal gadoids, such as the poor cod, lack these muscles. It is suggested that the sonic apparatus was present in the early species of the gadoids, with some species having lost their sonic ability. Interestingly, silent gadoids are mainly small schooling fishes. Gadoid species are most sensitive to sounds from 30 to 500 Hz. Gadoid hearing can be masked by ambient sound but also by anthropogenic sounds, which may therefore adversely affect their reproduction, with potential effects upon discrete local stocks. Listening for gadoid sounds provides a reliable, non-invasive way of locating spawning sites, which can enhance the protection of reproducing fish from human impacts.

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.

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.

Effects of Sound on the Behavior of Wild, Unrestrained Fish Schools.

To assess and manage the impact of man-made sounds on fish, we need information on how behavior is affected. Here, wild unrestrained pelagic fish schools were observed under quiet conditions using sonar. Fish were exposed to synthetic piling sounds at different levels using custom-built sound projectors, and behavioral changes were examined. In some cases, the depth of schools changed after noise playback; full dispersal of schools was also evident. The methods we developed for examining the behavior of unrestrained fish to sound exposure have proved successful and may allow further testing of the relationship between responsiveness and sound level.

Auditory Evoked Potential Audiograms Compared with Behavioral Audiograms in Aquatic Animals.

Auditory evoked potentials (AEPs) have become popular for estimating hearing thresholds and audiograms. What is the utility of these measurements? How do AEP audiograms compare with behavioral audiograms? In general, AEP measurements for fishes and marine mammals often underestimate behavioral thresholds, but comparisons are especially complicated when the AEP and behavioral measures are obtained under different acoustic conditions. There is no single representative relationship between AEP and behavioral audiograms and these audiograms should not be considered equivalent. We suggest that the most valuable comparisons are those made by the same researcher using similar acoustic conditions for both measurements.

"Large" Tank Acoustics: How Big Is Big Enough?

In this paper, we discuss the issues encountered when trying to perform hearing experiments in water-filled tanks that are several meters in lateral extent, typically large in terms of the size of the animals under study but not necessarily so with respect to the wavelengths of interest. This paper presents measurements of pressure and particle motion fields in these "large" tanks. The observed characteristics and complexities are discussed in reference to their potential impact on the planning and interpretation of hearing experiments.

Effects of Seismic Air Guns on Pallid Sturgeon and Paddlefish.

Pallid sturgeon and paddlefish were placed at different distances from a seismic air gun array to determine the potential effects on mortality and nonauditory body tissues from the sound from a single shot. Fish were held 7 days postexposure and then necropsied. No fish died immediately after sound exposure or over the postexposure period. Statistical analysis of injuries showed no differences between the experimental and control animals in either type or severity of injuries. There was also no difference in injuries between fish exposed closest to the source compared with those exposed furthest from the source.

Parvulescu Revisited: Small Tank Acoustics for Bioacousticians.

Researchers often perform hearing studies on fish in small tanks. The acoustic field in such a tank is considerably different from the acoustic field that occurs in the animal's natural environment. The significance of these differences is magnified by the nature of the fish's auditory system where either acoustic pressure (a scalar), acoustic particle velocity (a vector), or both may serve as the stimulus. It is essential for the underwater acoustician to understand the acoustics of small tanks to be able to carry out valid auditory research in the laboratory and to properly compare and interpret the results of others.

Auditory sensitivity in aquatic animals.

A critical concern with respect to marine animal acoustics is the issue of hearing "sensitivity," as it is widely used as a criterion for the onset of noise-induced effects. Important aspects of research on sensitivity to sound by marine animals include: uncertainties regarding how well these species detect and respond to different sounds; the masking effects of man-made sounds on the detection of biologically important sounds; the question how internal state, motivation, context, and previous experience affect their behavioral responses; and the long-term and cumulative effects of sound exposure. If we are to better understand the sensitivity of marine animals to sound we must concentrate research on these questions. In order to assess population level and ecological community impacts new approaches can possibly be adopted from other disciplines and applied to marine fauna.

Responses of free-living coastal pelagic fish to impulsive sounds.

The behavior of wild, pelagic fish in response to sound playback was observed with a sonar/echo sounder. Schools of sprat Sprattus sprattus and mackerel Scomber scombrus were examined at a quiet coastal location. The fish were exposed to a short sequence of repeated impulsive sounds, simulating the strikes from a pile driver, at different sound pressure levels. The incidence of behavioral responses increased with increasing sound level. Sprat schools were more likely to disperse and mackerel schools more likely to change depth. The sound pressure levels to which the fish schools responded on 50% of presentations were 163.2 and 163.3 dB re 1 µPa peak-to-peak, and the single strike sound exposure levels were 135.0 and 142.0 dB re 1 µPa(2) s, for sprat and mackerel, respectively, estimated from dose response curves. For sounds leading to mackerel responses, particle velocity levels were also estimated. The method of observation by means of a sonar/echo sounder proved successful in examining the behavior of unrestrained fish exposed to different sound levels. The technique may allow further testing of the relationship between responsiveness, sound level, and sound characteristics for different types of man-made sound, for a variety of fish species under varied conditions.

Fish hearing "specialization" - a re-evaluation.

Investigators working with fish bioacoustics used to refer to fishes that have a narrow hearing bandwidth and poor sensitivity as "hearing generalists" (or "non-specialists"), while fishes that could detect a wider hearing bandwidth and had greater sensitivity were referred to as specialists. However, as more was learned about fish hearing mechanism and capacities, these terms became hard to apply since it was clear there were gradations in hearing capabilities. Popper and Fay, in a paper in Hearing Research in 2011, proposed that these terms be dropped because of the gradation. While this was widely accepted by investigators, it is now apparent that the lack of relatively concise terminology for fish hearing capabilities makes it hard to discuss fish hearing. Thus, in this paper we resurrect the terms specialist and non-specialist but use them with modifiers to express the specific structure of function that is considered a specialization. Moreover, this resurrection recognizes that hearing specializations in fishes may not only be related to increased bandwidth and/or sensitivity, but to other, perhaps more important, aspects of hearing such as sound source localization, discrimination between sounds, and detection of sounds in the presence of masking signals.

Taking the Animals' Perspective Regarding Anthropogenic Underwater Sound.

Anthropogenic (man-made) sound has the potential to harm marine biota. Increasing concerns about these effects have led to regulation and mitigation, despite there being few data on which to base environmental management, especially for fishes and invertebrates. We argue that regulation and mitigation should always be developed by looking at potential effects from the perspectives of the animals and ecosystems exposed to the sounds. We contend that there is currently a need for far more data on which to base regulation and mitigation, as well as for deciding on future research priorities. This will require a process whereby regulators and researchers come together to identify and implement a strategy that links key scientific and regulatory questions.

Effects of sound exposure from a seismic airgun on heart rate, acceleration and depth use in free-swimming Atlantic cod and saithe.

Airguns used for offshore seismic exploration by the oil and gas industry contribute to globally increasing anthropogenic noise levels in the marine environment. There is concern that the omnidirectional, high intensity sound pulses created by airguns may alter fish physiology and behaviour. A controlled short-term field experiment was performed to investigate the effects of sound exposure from a seismic airgun on the physiology and behaviour of two socioeconomically and ecologically important marine fishes: the Atlantic cod (Gadus morhua) and saithe (Pollachius virens). Biologgers recording heart rate and body temperature and acoustic transmitters recording locomotory activity (i.e. acceleration) and depth were used to monitor free-swimming individuals during experimental sound exposures (18-60 dB above ambient). Fish were held in a large sea cage (50 m diameter; 25 m depth) and exposed to sound exposure trials over a 3-day period. Concurrently, the behaviour of untagged cod and saithe was monitored using video recording. The cod exhibited reduced heart rate (bradycardia) in response to the particle motion component of the sound from the airgun, indicative of an initial flight response. No behavioural startle response to the airgun was observed; both cod and saithe changed both swimming depth and horizontal position more frequently during sound production. The saithe became more dispersed in response to the elevated sound levels. The fish seemed to habituate both physiologically and behaviourally with repeated exposure. In conclusion, the sound exposures induced over the time frames used in this study appear unlikely to be associated with long-term alterations in physiology or behaviour. However, additional research is needed to fully understand the ecological consequences of airgun use in marine ecosystems.