The Impact of Underwater Sound on Aquatic Animals – And Especially Fishes

Underwater sound sources have been reviewed by Popper ¹⁸. Ships in the sea, lakes and rivers can be very noisy. The sounds generated by the vessels propagate along the surface, down into the water column, and can arrive close to the substrate. Variable sound levels and spectra are generated at different distances and depths. The sounds are generated by the ship engines, rotation of the propellers, and the creation of water flow and turbulence. In addition, many ships may also have other systems attached to them that can generate sound. For example, some have trawls that are towed across the seabed; sonar systems that are used to look at fishes and the seabed; and seismic air gun arrays towed by the ship that generate low frequency impulsive sounds that are used to detect oil and gas locations. The seismic air gun arrays not only generate sound in the water, they can also produce substrate vibration. They generate “ground roll”, a substrate vibration wave that occurs at the sea-floor (fluid/solid interface) and travels along the surface of the seabed. The wave is of maximum intensity at the interface and decreases exponentially away from the interface into both the water and the substrate solid medium. The ground roll wave travels slower than the speed of sound, but may travel considerable distances.

The offshore oil and gas facilities may be noisy themselves as they operate, and also sounds and substrate vibration may be generated when the facilities are constructed by drilling, and other activities. Very loud sounds, and high levels of substrate vibration are generated by Pile Driving (Figure 3) – which is used for the installation of bridges, quays and offshore structures including oil and gas facilities and wind turbines ⁶. Some offshore installations can require extensive pile driving over several weeks.

Figure 3.(Drawn by me): Pile driving, where a strong and rigid pile is banged from above, resulting in sound propagation through the seabed as well as through the water. Pile driving is used for construction work close to the shore and also within the sea. Below-ground impact produces compression waves which propagate outwards. Shear waves and interface waves are also produced. Propagation velocities are highest for the compression waves, intermediate for shear waves, and lowest for interface waves. As the waves propagate away from the pile they begin to separate. In addition, they can decay at different rates but this decay is frequency dependent. Interface waves at the lower frequencies may dominate substrate transmission at long distances, showing the least attenuation

The actual operation of Wind Turbines and Oil and Gas Systems also generates sound and vibration. It has been confirmed that the wind turbines radiate sound mainly at a few dominating frequencies from 30 Hz up to 800 Hz ¹. At frequencies below 30 Hz no contribution from the turbines can be detected due to the high background level from the waves and the low tower vibration level. Sounds are transmitted into the water via the vibration of the tower structure and vibration is also passed into the substrate. Wind farms are now being placed within the sea in many parts of the World. There is a real need to do some research on the possible adverse effects of wind farm construction and operation upon fishes and invertebrates. It is often suggested that the use of wind farms has enormous potential to deal with the current problems of climate change, by replacing more damaging energy sources. However, many marine fishes and invertebrates live within the parts of the sea, some near the seabed, where wind farms are likely to be built. In addition, migratory species like the salmon, sea trout and eels swim to and from rivers along the coast, and are likely to pass through mid-water areas occupied by offshore wind farms, some of which float on the water surface. There is now a real need to obtain data on the impact of offshore wind farms upon fishes and invertebrates, as our current knowledge is rather poor. Electric cables are used to to convey the power generated by marine renewable energy installations to electrical sub-stations. The power cables are often installed across the sea, into coastal bays and even river mouths, and they connect the wind farm turbines to the mainland, and it is important to consider the potential effects of the Electrical and Magnetic Fields (EMFs) they generate upon marine species. A study at Heriot-Watt University in Edinburgh showed that lobster and crab eggs and larvae were deformed by the power cables. It is possible that the cables can result in animals being exposed to EMFs in three ways: the electric field produced by the voltage applied to the cables; the magnetic field produced by current flow on the cable; and an indirect AC electric field induced by alternating magnetic fields from the cables or movement through a DC field of the earth or cables ¹⁹. It may be best to bury the power cables well under the seabed.

Underwater sounds are very important to fishes and aquatic invertebrates. They especially use sounds to navigate through the water and to detect signals from natural environment sources, and from other animals. Some of the fishes are entirely pelagic, for example the herring (Clupeiformes), while others are benthopelagic, for example the cod and haddock (Gadiformes), while a few species are entirely benthic, including the flatfishes (Pleuronectiformes), and many of the invertebrates. The vision ability of these animals in the water is generally poor and they use the “acoustic scene” to locate natural underwater features including preferred habitats, as well as their prey and predators, and they also use sound to set their orientation during migration. Sound travels further and faster in all directions through water than it does through the air and it allows aquatic animals to detect natural sources, and to communicate well with one another. Underwater sound is highly relevant to many aquatic animals ⁵. They listen to the “acoustic scene” and use this to orientate and navigate. Fishes mainly have ears that are sensitive to particle motion. There are two fish ears within the skull, each containing 3 otolith organs, the saccule, utricle and lagena (Figure 4), each of these organs containing a heavy mass (the otolith itself) and sensory hair cells that respond to the motion of the otolith. The fish itself, and the sensory tissues have approximately the same density as water and move back and forth in a sound field. However, the otolith is much denser and moves with a different amplitude and phase resulting in the hair cell bundles that are in contact with the otolith being subjected to a directional shearing force. However, some fishes have their gas-filled swim bladder close to the ear, where sound pressure causes volume oscillations which are transferred to the inner ear, often via a physical connection, e.g. through paired bladder extensions, additional air cavities or a series of bones. The compression of the swim bladder by sound pressure can therefore generate particle motion close to the ear, especially at higher frequencies, stimulating the otolith organs and enabling such species to detect the sound pressure as well as the particle motion. Aquatic Invertebrates are especially sensitive to particle motion. For example, the Lobster has hair fan organs that respond to particle motion, giving them low frequency audiograms. Of course, aquatic animals do not hear all frequencies within their functional hearing range. They are more sensitive to some frequencies than others. It is important to examine their audiograms.

Figure 4.(Drawn by me): The otolith organs of a fish, the cod. Each otolith (yellow) is a heavy calcareous lump, sitting on a membrane (pink) of sensory hair cells. The head of the fish is moved by the particle motion but the dense otoliths tend to move less, resulting in motion of the sensory hair cells. The hair cells in different parts of the air are orientated in different directions.

Many marine mammals, fishes and invertebrates make sounds themselves. Amongst the vocal fishes are some of the most abundant and important commercial fish species, including the cod & haddock (Gadidae). Many gadoid fishes make underwater sounds, but the sounds differ between species. Some produce knocking sounds, while others produce grunts. In all cases the sounds are pulsed, with each pulse generated by the contraction of a pair of Drumming Muscles attached to the gas-filled swim bladder (Figure 5). The muscles show very fast contraction.

Figure 5.(Drawn by me) The sound producing muscles of fishes are often attached to the gas-filled swim bladder, as they are here in the haddock. a is viewed from above, and b from the front, behind the head. The muscles are rather large and powerful, and the gas within the swim bladder is easily compressed by them, generating sound pressure.

The sounds produced by haddock, especially during courtship and mating, have been recorded and analyzed in the aquarium and in the sea ^{8, 9}. The haddock produce sounds when they are feeding, mating, or fighting and they also make noises associated with swimming. They produce species-specific sounds, and even individual-specific sounds. Their sounds are often loud and may dominate sound in the water.

Fish sounds can vary in structure depending on the mechanism used to produce them, but they are generally composed of low frequencies, with most of their energy lying below 3 kHz. So far, no no high frequency sounds have been recorded from fish, although marine mammals can produce ultrasonic sounds. Many fishes, including the Atlantic cod and haddock make sounds during their spawning behavior. The male haddocks accumulate at particular spawning locations and use sounds to attract the females, and to advertise their occupation of a spawning The sounds are often varied during their spawning. For example, the male haddock makes sounds to attract females, and thousands of males gather together on the seabed making their sounds. The females are attracted and then select a particular male to spawn with, discriminating males with different characteristics through sound detection. The sounds of individual male haddock can readily be distinguished. The male haddock varies its sounds during the spawning behaviour, while the female remains silent during spawning, but can make sounds normally. The different sounds produced by the male are shown in Figure 6.

Figure 6.(Drawn by me) The sounds made by male haddock during spawning. Starting at the bottom the males make repeated knocks on the seabed. When the female arrives and selects a particular male, that male leads the female up through the water and produces faster sounds, and it then mounts the female to spawn, producing sounds initially but then becoming silent when the female releases its eggs and the male adds its sperm into the water. The sperm and eggs combine to generate a new young fish.

The differences between the sounds of different males on the seabed may enable females to select particular males. The sounds may also allow males to assess the strengths of other competing males. Each individual male may then join a female, and engage in spawning with it, making some specialized sounds at the start of the mating behavior. The male that is chosen then flaunts the female with a new sound, and then mounts the female to spawn but later becomes silent. The male and female embrace one another and release their eggs and sperm into the water to create juvenile haddock. However, human noise-making activities may affect spawning success by masking the haddock calls and driving haddock away from their spawning grounds.

Many other important fishes also make sounds in the sea, including: cod, pollack, gurnards, bullheads, gobies, and blennies. However, there have been very few studies of sound producing fishes in the sea. lakes and rivers. Marine mammals, including whales and seals, that often prey upon fishes, also make sounds in the sea; and some invertebrates, including squid, lobsters, sea urchins, and some crabs, also make sounds. It is important for the management of fisheries for species like the haddock to determine where the stocks spawn. Listening with a hydrophone from a relatively quiet travelling ship is an effective non-invasive way of locating spawning fishes and mapping their spawning grounds. The sites where haddock and other fish species spawn and the factors that bring the fish together to spawn at particular locations are often not well known. Haddock spawning in the sea has been located by listening for the sounds this species makes during its reproductive behavior. The characteristics of the sounds made by haddock were first examined in the aquarium ². Reproductive behavior was monitored in an aquarium for 3 months over each of two successive spawning seasons. The observations showed that male haddock were territorial and that visits to their territories by females triggered courtship behavior, leading to spawning. Entry of females to the territories was induced by the sounds made by the males. Later, listening was then carried out in a Norwegian fjord (Figure 7), ³, where fishers were concerned to find spawning haddock.

Figure 7.(Drawn by me) The sounds made by haddock during spawning at Balsfjord, north of the Arctic Circle near Tromso in northern Norway. The males made repeated knocks on the seabed, and were located using a hydrophone hanging beneath a ship. Their presence is shown in the blue areas.

Long sequences of repeated knocks were heard in the fjord, similar to the display sounds recorded by male haddock during stereotyped reproductive behavior in the aquarium. Rapidly repeated knocks and humming were also heard, confirming that fish were engaging in courtship. At night the sounds merged into a continuous low frequency rumble, suggesting that many haddock were present, producing sounds simultaneously. Listening for haddock sounds provides a reliable, non-invasive way of locating aggregations of spawning haddock in the sea, allowing closer definition of the spawning areas. Both fishing and exposure of haddock to man-made noise at the critical time of spawning may have severe detrimental effects upon their reproductive success.

Fishes and invertebrates can hear very well. They are especially sensitive to the particle motion but some are also sensitive to the sound pressure. Listening to natural sounds in their environment can be critical for their survival and reproduction. Their hearing abilities are usually expressed in terms of hearing thresholds (their auditory thresholds at different frequencies). Conditioning experiments involve training the animals to respond every time a sound is presented. Once a response has been established the sound level can then be progressively lowered until the animal no longer responds, enabling the auditory threshold to be determined. The threshold is the sound level at a particular frequency, that is audible to an animal under quiet background conditions. Plotted as a function of frequency it provides the Audiogram. Electrophysiological methods register auditory evoked potentials (AEP) or auditory brainstem responses (ABR) by monitoring hair cell or brain responses. Most of the hearing thresholds are generally determined using pure tone sounds, at a number of frequencies. Only a small number of fishes and invertebrates have had their audiograms measured. Many of the audiograms are determined while measuring the sound pressure. However, it has been shown that the cod detects particle motion at frequencies below 100 Hz, and only at higher frequencies detects the sound pressure ⁴. It is important to monitor the particle motion, as well as the sound pressure, when examining the hearing abilities of fishes and invertebrates. In addition to examining the hearing thresholds in aquatic animals it is also important to examine those sound levels that may damage their auditory systems and impair the detection of sounds.

Most hearing studies have been carried out in small aquariums in the laboratory, where the sound fields are highly complex as a result of the presence of pressure-release surfaces, and where it is almost impossible to set up and calibrate a reliable acoustic field with evident levels of particle motion. The particle motion components of the sound field are therefore, often completely ignored. Furthermore, background noise is often high over a wide range but especially at the lower frequencies and may mask the playback of sounds ¹⁰. Background noise levels should therefore be considered in determining auditory thresholds and preparing an audiogram, but this has rarely been done. Some of the most interesting hearing experiments have been carried out in mid-water in the sea, where it is possible to estimate the particle motion levels by monitoring the sound pressure ¹².

The presence of adverse underwater sounds (often termed “noise”), and also substrate vibration, generated by human activities (anthropogenic sources) can be quite harmful to fishes and aquatic invertebrates, as the detection of sounds of interest to the animals can be adversely influenced by the presence of noises, whether the noises are natural sounds or sounds from human sources. The abilities of fishes and invertebrates to use sound to navigate, detect predators and prey, select habitat types, and communicate with one another, may be strongly affected by exposure to other sounds (noise). The noise may cause physical damage to the body tissues; damage to the auditory tissues, including the sensory hair cells; and changes to important behavior patterns, adversely affecting feeding migrations, and spawning. Masking of biologically important sounds, including those from the same species, may also be detrimental, the unwanted sound (the masker) decreases the ability to detect important natural sounds.

Many major developments are now taking place off our coasts, including: harbor re-developments; offshore oil and gas systems; offshore wind farms, fixed and floating tidal energy generators; and wave energy generators. Noise levels in the sea, lakes and rivers have been changing dramatically as a result of human activities, and may have adverse effects upon aquatic animals. The sea, lakes and rivers are relatively dark, low-visibility environments, where sound is especially important to the aquatic animals.

The effects of sound on the aquatic animals vary with distance from the source. However, modelling of particle motion levels at different distances from the source is rarely carried out in Impact Assessments. Models have recently been developed for dealing with ground roll generated by seismic surveys, but such models also need to be applied to pile driving and other sources of substrate vibration. Normally, assessments and modelling are only done in terms of sound pressure. Often: no mention is made of particle motion; no account is taken of substrate or interface waves; and sensitivity to Infrasound is often ignored. Infrasound consists of sound waves with a frequency below the lower limit of human audibility (generally 20 Hz). Hearing becomes gradually less sensitive as frequency decreases, so for humans and animals to perceive infrasound, the sound level must be sufficiently high.

It is evident that there are very substantial gaps in our knowledge about the effects of sound on all aquatic animals, and also a very substantial need for better understanding of the sounds produced by various sources and how they may affect aquatic animals. Great efforts are being directed at examining the effects of underwater noise upon marine mammals, but much less attention is being paid to effects upon fishes and invertebrates. Marine mammals make up perhaps 100 species, but there are over 32,000 species of fishes and a great number of marine invertebrates. It is important to establish Sound Exposure Criteria for fishes & invertebrates. However, environmental impact assessments of offshore activities often involve dubious assumptions. Sound exposure criteria are often assumed rather than based on real data. The metrics employed are often inappropriate, especially for fish and invertebrates, which are primarily sensitive to particle motion, but the effects of the particle motion are often ignored. Sound propagation models have seldom been validated and the sound pressure measurements do not always predict particle motion levels. They are especially poor for shallow water conditions or where sound travels through the substrate. Sound pressure measurements only tend to work well or estimating the particle motion in midwater in the sea ¹².

Any interference with the acoustic scene can have a negative impact upon aquatic animals. It is important to examine the hearing abilities of aquatic animals. Much work has been done on the hearing of fishes, especially those living in the sea. There are substantial differences in hearing sensitivity and frequency range between different fish species ¹⁸. Most are sensitive to Particle Motion and only some are sensitive to Sound Pressure.

It is necessary to determine the levels of sound that may harm animals, in terms of Particle Motion as well as Sound Pressure, for fishes and invertebrates, in order to develop criteria for the harm caused by sound exposure. Sound Exposure Criteria set limits to the received levels for particular sources, based on the levels above which damage or adverse effects may occur. The setting of such criteria was established initially for marine mammals ²⁰. However, only a few criteria have been established for fishes and invertebrates ¹⁷. Environmental Impact Assessments often emphasize that sounds, and especially low frequency sounds, do not travel well through shallow water. Although this is the case for sound pressure it may not be the case for particle motion. Particle motion levels in shallow water can be quite high, especially when sound is being transmitted through the seabed or the ground/water interface. There have been few measurements of the particle motion levels generated by human aquatic activities. The transmission of particle motion through the substrate is hardly ever considered in assessing effects upon aquatic fishes and invertebrates, despite its importance.

Based on currently available research, it is important to provide a firm scientific, technical basis on which to improve the current understanding of the sound levels that are associated with the very earliest onset of physical injury to fishes, especially from the exposure to impulsive underwater sound. There is a need to provide a firm scientific, technical basis on which to improve the identification of the effects upon fishes from exposure to impulsive underwater sound.

In setting the Sound Exposure Criteria, it is important to determine those sound pressure and particle motion levels that affect fishes and invertebrates adversely. At the highest sound level an animal may be killed or seriously injured by the forces associated with passage of the acoustic wave through its body. Assessments of killing or injury, damage to the body tissues, including damage to the auditory system, or physiological damage, are generally done using sound pressure only, and there is a need for experiments where fish and invertebrates are shaken by particle motion. rather than squeezed by sound pressure. Behavioural responses must ideally be examined using free-living fish and invertebrates in the sea rather than in aquarium tanks. Extensive reviews of Sound Exposure Criteria Guidelines have been cited in ^{11, 15, 16, 17}.

Where there are problems from human sounds upon animals is especially important to deal with the effects of noise – termed Mitigation. The intention of mitigation is to avoid sound exposure or to reduce it to levels that are harmless to the animals that might be exposed. One solution is simply to remove human noise sources from aquatic areas, including the sea, rivers, lakes and estuaries where they are likely to be damaging to aquatic animals. Another approach is to reduce the levels of sound that are being generated. Once they have been implemented, mitigation measures need to be assessed to ensure they have been effective. Ecological and environmental impact assessments or surveillance monitoring could generate basic understanding and provide important benefits to future developments and regulatory actions with respect to noise mitigation.