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

Abstract

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.

Keywords: behaviour; criteria; effects; guidelines; hearing; sound.

Figure 1

Fish hearing sensitivity (thresholds) obtained under open sea, free‐field, conditions in response to pure tone stimuli at different frequencies. The lower the thresholds (y‐axis), the more sensitive the fish is to a sound. Thus, Clupea harengus has best hearing of all of these species over a wider range of frequencies. Note that the thresholds in Gadus morhua and C. harengus obtained under quiet conditions may be below natural ambient noise levels, especially at their most sensitive frequencies. In the presence of higher levels of noise, the thresholds would be raised, a phenomenon referred to as masking. Gadus morhua and C. harengus are sensitive to both sound pressure and particle motion, whereas Limanda limanda and Salmo salar are only sensitive to particle motion. The reference level for the particle velocity is based on the level that exists in a free sound field for the given sound pressure level. n.b., For the particle velocity levels in this figure to match the sound pressure levels in a free sound field it is necessary to calculate an appropriate particle velocity reference level. If the standard reference levels are used, then the curves will not match one another and so they are not included here to keep the figure relatively simple. Fig. © 2018 Anthony D. Hawkins, all rights reserved

Figure 2

Masking in the Gadus morhua and Salmo salar by ambient noise. The thresholds were determined using a pure tone signal at a frequency of 160 Hz. The ambient noise (natural sea noise, augmented by white noise from a loudspeaker) is expressed as the spectrum level at that same frequency (dB re 1 μPa/Hz). Closed symbols, thresholds to natural levels of ambient noise; open symbols, thresholds to anthropogenic noise. n.b., The thresholds in S. salar were only influenced by high noise levels, above the natural ambient levels of noise (data from Hawkins, 1993). Fig. © 2018 Anthony D. Hawkins, all rights reserved

Figure 3

Schematic drawing of the ear of Gadus morhua (anterior is to the left): (a) top view of the body showing the location of the ears in the cranial cavity as well as the proximity of the rostral end of the swim bladder to the ear; (b) lateral and (c) top view of the same ear. Each ear is set at an angle relative to the midline of the fish. , The otolith organs, , the semicircular canals (enlarged areas are the ampullae regions that contain the sensory cells); , the dense calcarious otolith lying in close proximity to the sensory epithelium (). Also see Figure 4. Fig. © 2018 Anthony D. Hawkins, all rights reserved

Figure 4

A frontal view of the head of Gadus morhua showing a section of the saccule (). The saccular chamber is filled with perilymph and contains the otolith (), which lies close to the sensory hair cells of the epithelium (macula). The hair cells are innervated by the eighth cranial nerve. Fig. © 2018 Anthony D. Hawkins, all rights reserved

Figure 5

The sensory epithelia of the end organs of the inner ear have numerous mechanoreceptive sensory hair cells. The apical ends of these cells, directed into the lumen of the epithelia, have ciliary bundles (inserts in the figure) consisting of a single kinocilium (longest of the cilia) and graded stereocilia. Bending of the ciliary bundle during sound stimulation results in neurotransmitter release to stimulate the 8th cranial nerve. The sensory cells on the otolith maculae are organized into orientation groups, with all of the cells in each group having their kinocilia in the same general direction. In this typical saccular epithelium (anterior to the left, dorsal to the top), the cilia on the rostral end are oriented rostrally or caudally, while the cells on the caudal end are oriented dorsally and ventrally. , The approximate dividing lines between orientation groups)