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Information gaps in understanding the effects of noise on fishes and invertebrates

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Abstract

The expansion of shipping and aquatic industrial activities in recent years has led to growing concern about the effects of man-made sounds on aquatic life. Sources include (but are not limited to) pleasure boating, fishing, the shipping of goods, offshore exploration for oil and gas, dredging, construction of bridges, harbors, oil and gas platforms, wind farms and other renewable energy devices, and the use of sonar by commercial and military vessels. There are very substantial gaps in our understanding of the effects of these sounds, especially for fishes and invertebrates. Currently, it is almost impossible to come to clear conclusions on the nature and levels of man-made sound that have potential to cause effects upon these animals. In order to develop a better understanding of effects of man-made sound, this paper identifies the most critical information needs and data gaps on the effects of various sounds on fishes, fisheries, and invertebrates resulting from the use of sound-generating devices. It highlights the major issues and discusses the information currently available on each of the information needs and data gaps. The paper then identifies the critical questions concerning the effects of man-made sounds on aquatic life for which answers are not readily available and articulates the types of information needed to fulfill each of these drivers for information—the key information gaps. Finally, a list of priorities for research and development is presented.
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Reviews in Fish Biology and Fisheries
ISSN 0960-3166
Volume 25
Number 1
Rev Fish Biol Fisheries (2015) 25:39-64
DOI 10.1007/s11160-014-9369-3
Information gaps in understanding the
effects of noise on fishes and invertebrates
Anthony D.Hawkins, Ann E.Pembroke
& Arthur N.Popper
1 23
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REVIEWS
Information gaps in understanding the effects of noise
on fishes and invertebrates
Anthony D. Hawkins Ann E. Pembroke
Arthur N. Popper
Received: 3 February 2014 / Accepted: 18 August 2014 / Published online: 12 September 2014
Springer International Publishing Switzerland 2014
Abstract The expansion of shipping and aquatic
industrial activities in recent years has led to growing
concern about the effects of man-made sounds on
aquatic life. Sources include (but are not limited to)
pleasure boating, fishing, the shipping of goods,
offshore exploration for oil and gas, dredging, con-
struction of bridges, harbors, oil and gas platforms,
wind farms and other renewable energy devices, and
the use of sonar by commercial and military vessels.
There are very substantial gaps in our understanding of
the effects of these sounds, especially for fishes and
invertebrates. Currently, it is almost impossible to
come to clear conclusions on the nature and levels of
man-made sound that have potential to cause effects
upon these animals. In order to develop a better
understanding of effects of man-made sound, this
paper identifies the most critical information needs
and data gaps on the effects of various sounds on
fishes, fisheries, and invertebrates resulting from the
use of sound-generating devices. It highlights the
major issues and discusses the information currently
available on each of the information needs and data
gaps. The paper then identifies the critical questions
concerning the effects of man-made sounds on aquatic
life for which answers are not readily available and
articulates the types of information needed to fulfill
each of these drivers for information—the key infor-
mation gaps. Finally, a list of priorities for research
and development is presented.
Keywords Behavior Pile driving Seismic
airguns Shipping Fish Invertebrates
Introduction
Since the start of the Industrial Age, humans have
increasingly exploited aquatic environments. These
developments often involve the accidental or deliber-
ate generation of underwater sounds. Today, in the
early twenty-first century, these sources of sound have
become more diverse and have the potential to add
sound to large expanses of the aquatic environment.
Some sources result in a chronic increase in low level
background noise over extended periods of time,
effectively masking sounds of interest to aquatic
animals or having other behavioral effects. Other
sources, while taking place over shorter periods, are
more intense and have the potential to kill or injure
A. D. Hawkins
Loughine Ltd, Kincraig, Blairs, Aberdeen AB12 5YT, UK
A. E. Pembroke
Normandeau Associates, 25 Nashua Road, Bedford,
NH 03110, USA
A. N. Popper (&)
Department of Biology, University of Maryland,
College Park, MD 20742, USA
e-mail: apopper@umd.edu
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Rev Fish Biol Fisheries (2015) 25:39–64
DOI 10.1007/s11160-014-9369-3
Author's personal copy
aquatic animals as well as alter their behavior (e.g.,
Slabbekoorn et al. 2010).
Sources of man-made sound in water have been
discussed extensively in the literature (e.g., Hawkins
et al. 2008; Popper and Hastings 2009; Popper et al.
2014; Popper and Hawkins 2012; Hawkins and Popper
2014; Normandeau 2012). In brief, the sources include
(but are not limited to): pleasure boating; fishing,
shipping; geophysical surveys for oil and gas; dredg-
ing; construction of bridges, harbors, oil and gas
platforms, wind farms and other renewable energy
devices; and the use of sonar by commercial and
military vessels.
There is growing concern about the effects of these
man-made sounds on aquatic life. It has been pointed
out that there are very substantial gaps in our
understanding of effects of these sounds (e.g., Popper
and Hastings 2009; Normandeau 2012; Hawkins and
Popper 2014; Popper et al. 2014). Much of the
information on effects currently comes from ‘‘gray
literature’’ reports that have not been peer reviewed,
are often anecdotal, and lack detail on experimental
design and controls.
Reading the literature on effects of sounds, partic-
ularly as it relates to fish, invertebrates, and turtles, it is
clear that there are so many information gaps that it is
almost impossible to come to clear conclusions on the
nature and levels of man-made sound that have
potential to cause changes in animal behavior or even
physical harm. There is strong interest in developing
such sound exposure criteria by investigators, regula-
tors, and industry (e.g., Woodbury and Stadler 2008;
Stadler and Woodbury 2009; Popper et al. 2014), but,
to date, the criteria proposed have not been based on
substantive data. The most comprehensive recent
attempt at reviewing the data has drawn only limited
conclusions on those sound levels that might affect
fish and turtles (Popper et al. 2014). No setting of
criteria has even been attempted for aquatic inverte-
brates since so little is known about effects of man-
made sound on these animals.
Because of the substantial lack of knowledge on
effects of man-made sounds, and because of limited
funding and facilities to undertake appropriate
research it is important to consider priorities in terms
of the kinds of information required. The purpose of
this paper is to identify the major information gaps in
what we know about effects, and then set priorities for
future work. The origin of this analysis was a public
workshop supported by the US Bureau of Ocean
Energy Management (BOEM) Environmental Studies
Program, held in March 2012 ‘to identify the most
critical information needs and data gaps’’ on the
effects of various man-made sound on fishes, fisheries,
and invertebrates resulting from the use of sound-
generating devices by the energy industry (Norman-
deau 2012). This review is based on that analysis but
encompasses all sound sources and their effects on
fishes and invertebrates: it is not limited to sound
generated by the energy industry. Many of the
examples provided are taken from marine and coastal
waters, as there is a paucity of good science for other
waters, but the concepts presented most likely apply to
freshwater systems as well.
It is not the goal of this paper to present a
comprehensive review of the material that resulted
in identification of major gaps. Instead, we have been
selective in choosing citations to document the gaps.
For more comprehensive reviews readers are directed
at the aforementioned papers. This review is strongly
influenced not only by the extensive work reported in
the Normandeau report to BOEM, but also by other
meetings that the authors have participated in (and
often organized—e.g., Hawkins et al. 2008; Popper
and Hawkins 2012,2015; Popper et al. 2014). While
the suggestions made in this review belong to the
authors, they have benefitted from discussions with
colleagues from around the world. Although they will
not be mentioned by name, for fear of missing some,
their contributions are gratefully acknowledged.
Goals of this analysis
The goal of Gap Analysis is to define the present state
of knowledge, the desired or ‘target’ state of knowl-
edge, and the gaps between them. This analysis asks:
Where are we now in our knowledge of the effects
of man-made sound on marine and coastal fishes
and invertebrates?
Where do we want to be?
What must be put in place so that the desired target
state can be reached?
This gap analysis sets out to highlight those
requirements that are being met and those that are
not. It provides a foundation for deciding what is
required to achieve a particular outcome.
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For each topic considered in this review, an attempt
has been made to:
Define information needs about effects of noise on
fishes and invertebrates
Consider which of those needs are currently being
met
Examine those needs that are not being met and
how they might be met
Suggest research that might have high priority for
future funding
Organization of the analysis
Definitions of terms used in this analysis are provided
in Text Box 1, and the discussion of information in the
analysis is divided into several major topics. Along
with each brief discussion, a table, representing the
heart of the analysis, is presented for each topic. In the
tables, the left-hand column (‘‘Drivers for Information
Acquisition’’) describes the underlying concerns or
actions that raise the questions for which answers are
not readily available from existing research. The right-
hand column (‘‘Information Gaps’’) articulates the
types of information that would be needed to fulfill
each driver. There are a number of recurrent themes—
questions that arise under more than one topic.
The analysis is followed by a list of priorities for
research and development. Priorities on this list have
been defined in terms of those that are achievable,
have the most relevance, and have the greatest
potential to advance our understanding of the impact
issues in the reasonable future. The far broader
research questions listed in the Gap Analysis itself
provide a picture of where, over the next decade, the
field should go. Addressing these broader research
questions will be the responsibility of many groups
around the world.
Topic 1: background levels of sound in the sea
Existing environmental conditions must be considered
in those sea areas likely to be affected by develop-
ments that generate underwater sound (Knudsen et al.
1948). There are few historical records of levels of
sound in the sea. On the rare occasions that systematic
measurements of sound in the sea have taken place, it
has often been at local sites and the records are often
incomplete or unpublished.
A significant number of ambient noise measure-
ments were obtained in deep water during the first half
of the twentieth century. Knudsen et al. (1948) showed
that at frequencies between 200 Hz and 50 kHz the
level of ambient noise is dependent upon sea-state.
The underlying physical processes that result in this
variation are incompletely understood, but flow noise
from surface wind, breaking waves, and bubble
formation is thought to be important. Wenz (1962)
confirmed that in the frequency region above 100 Hz
the ambient noise level depends on weather condi-
tions, with wind and waves creating sound. The level
is related to the wind speed and decreases with
increasing frequency above approximately 500 Hz. At
frequencies around 100 Hz, distant shipping makes a
significant contribution to ambient noise levels in
almost all the world’s oceans.
The data from Wenz (1962), Knudsen et al. (1948)
are generally accepted as providing overall indications
of the range of sea noise levels and the source of the
dominant noise in each frequency range. Cato (1992)
has also contributed to our knowledge of biological
contributions to the ambient noise. However, their
measurements were undertaken at particular times and
places and often in relatively deep-water environ-
ments. Fewer data have been published for shallow
coastal waters and estuarine environments, and hardly
any for freshwater environments. Relatively little is
known about the range of sounds associated with
particular habitats and the contributions made to the
soundscape by different biotic and abiotic sources. A
consistent approach to measuring and reporting the
characteristics of underwater soundscapes is essential
to understanding how aquatic biota are affected by
sounds, both natural and man-made. McWilliam and
Hawkins (2014) have pointed out that soundscape
interpretation is still at a developmental stage.
Advancing understanding of the spatial dynamics of
soundscapes in underwater habitats has the potential
for better understanding of ecosystem processes,
particularly how spatial patterns of recruitment may
have developed and how migratory species may
navigate by the detection of acoustic features within
the environment (Simpson et al. 2004; Mann et al.
2007; van Parijs et al. 2009; Radford et al. 2010;
Bittencourt et al. 2014; Gage and Axel 2014).
Rev Fish Biol Fisheries (2015) 25:39–64 41
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A review of marine underwater noise Hildebrand
(2009) cites the data of Mazzuca (2001), which
suggests an overall increase of 16 dB in low frequency
noise during the period from 1950 to 2000, corre-
sponding to a doubling of noise power (3 dB increase)
in every decade for the past five decades. In some parts
of the ocean it is known that man-made sound has been
increasing across much of the frequency spectrum
(Andrew et al. 2002; McDonald et al. 2008), especially
at lower frequencies (\500 Hz) (Frisk 2007). Indeed,
at these frequencies, the level of sound above back-
ground may serve as an indicator of the degree of
industrialization of the ocean. The volume of cargo
transported by sea has been doubling approximately
every 20 years, and it is likely that this has resulted in
an overall increase in sound levels at many locations.
Offshore oil and gas exploration and production, as
well as renewable energy developments, have also
expanded over the same period.
Currently, there are insufficient measurements of
aquatic sound levels to understand how they have
changed over past decades. There is a total absence of
data on sound levels in aquatic ecosystems that pre-date
the increase of man-made sound levels in the 1900s.
Perhaps more critically there is an absence of long-data
sets that indicate changes in sound levels over time. There
are few measurements to adequately describe or quantify
aquatic noise on a global scale. The long-term variation of
sound in aquatic environments is a fundamental knowl-
edge gap. Long time series of sound levels are required at
a range of locations including not only those exposed to
increasing levels of man-made sound but also areas that
are representative of quiet conditions or are dominated by
sounds of biological origin (Table 1).
Text Box 1 Concepts and terms (in bold) critical for understanding this review
Noise is used colloquially to describe unwanted sound that interferes with detection of other sounds of interest. Noise is also used
to describe background levels of sound in the sea, including the naturally occurring and spatially uniform sounds generated by
distributed biological sources, weather events, and/or physical phenomena that cannot be assigned to individual sources. In this
paper the term sound, rather than noise, is used to refer to identifiable man-made sources, such as ships or oil and gas platforms, or
distant man-made sources that cannot be located. Where others have used the term ambient noise or background noise to describe
naturally occurring sounds from distributed sources then that usage will also be followed
The term soundscape is used in this review to describe the physical sound field at a particular time and place. The term does not
consider the sound field as experienced or perceived by any organism living there
In considering effects of sound (or any stimulus) on organisms, reference is made to acute or chronic effects. Acute effects may
result in mortal or potentially mortal injury to animals as well as sudden changes in behavior. Death may occur immediately upon
exposure to a stimulus, or at some time afterwards due to the actual damage imposed or reduced fitness that leads to predation on
the affected animal. Chronic effects refer to long-term changes in the physiology and/or behavior of an animal. These generally do
not lead to mortality themselves, but they may result in reduced fitness leading to increased predation, decreased reproductive
potential, or other effects. Acute effects are generally the result of very intense (loud) sounds. Exposure to the individual sounds is
often of short duration. In many instances these sounds are repeated. Acute effects may also arise from large changes in the
hydrostatic pressure generated by explosions and other sources. Such adverse effects may also be described as barotrauma (see
Stephenson et al. 2010; Carlson 2012; Halvorsen et al. 2011,2012a)
Chronic effects result from exposure to both continuous sound and intermittent sound over long time periods, not necessarily at
high levels, and may result from increased shipping or other human activities. The sounds resulting in chronic effects are often
continuously generated over large areas, where the overall background level of sound in the area is higher than the natural
background level
Cumulative effects arise from the temporal repetition and accumulation of effects from a single type of source—for example the
repeated strikes of a pile driver. In-combination effects, also described as synergistic effects or aggregate effects, arise from the
accumulation of effects from a number of different types of stressors—for example, from sounds from different sources or from
the combined effects of sound exposure, water contamination, and fishing (e.g., Johnson 2012). U.S. National Environmental
Policy Act (NEPA) analyses consider both cumulative and in-combination effects, as defined here, as cumulative impacts
There is often uncertainty about the use of ‘impact’’ and ‘‘ effect.’’ They are often used synonymously, but it is clear that there are
subtle differences in meaning by different authors. A more specific usage has been adopted here. ‘‘Impact’’ refers to a causal
agent, such as the sound from a seismic operation or the wake from a ship. ‘‘Effect’’ means the resultant response of or on an
animal or population
Finally, man-made is to be seen as synonymous with human-made and anthropogenic as used in other literature and is gender-
neutral
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Topic 2: sources of man-made sound
Underwater noise needs to be understood and modeled
in terms of the spatial and temporal fields generated by
different sound sources, both natural and man-made.
Together with propagation characteristics, such infor-
mation enables an inventory to be developed—to
contribute to the building of soundscapes for an area.
Comprehensive numerical models of the sound field
are required, based on knowledge and measurements
of the sources and of the propagation environment.
Such models can be used to explore the relative
significance of different sources, guide design of
further measurements, and provide tools for planning
mitigation efforts where necessary.
To model sound fields it is necessary to know the
distinctive characteristics of individual sources in
order to examine their effects upon animals and
habitats. There are many different man-made sound
sources in aquatic environments, and they can be quite
complex in their characteristics (reviewed in Popper
and Hawkins 2012,2015; Popper et al. 2014). Some of
these, such as explosions, seismic air guns, and impact
pile driving have the potential to add to acute noise
exposure since they produce sounds that are impulsive
and very intense, particularly close to the source. In
contrast, sounds produced by ‘‘quieter’’ sources such
as operating wind farms and vessels provide chronic
exposure. The sounds continue for long periods of
time (perhaps even indefinitely) although they are
generally not nearly as loud as impulsive sources.
Explosions
Explosives are used underwater in a wide range of
applications including the construction or removal of
installations such as offshore oil platforms. Explosions
differ in a number of ways from low-amplitude point
sources of sound (Weston 1960). During an underwa-
ter explosion a spherical shock wave is produced along
with a large oscillating gas bubble that radiates sound.
The shock pulse has rapid rise time and exponential
Table 1 Background levels of sound in the sea
Drivers for information acquisition Information gaps
There is strong interest in describing and characterizing
soundscapes in different parts of the ocean, including inshore
waters as well as other aquatic environments. How do these vary
by locale, season, time of day, weather conditions, etc.? Aquatic
soundscapes are the result of:
Ambient sounds generated by physical factors;
Biological sounds;
Man-made sounds; and
The local sound transmission regime
Ambient noise is site specific, and more data are required on the
soundscapes associated with different habitats and ecological
niches
Appropriate methods for the measurement, description and
analysis of soundscapes will be critical in the future for
identifying trends in level and characteristics of the acoustic
environment. There is currently no archive for recordings, no
protocol for making such measurements, and few analyses of
natural soundscapes performed to specified standards
Monitoring of soundscapes before, during, and after the new
developments, like the construction and operation of wind farms,
is needed, but is rarely carried out. Most observations on
soundscapes have been incidental to other activities. Results of
monitoring that has taken place are not generally made publicly
available There is a need for a repository of data on soundscapes
and the sharing of such data
Presentation of noise budgets can be difficult to interpret,
depending on the units used to derive them
Definition of those physical quantities and metrics that are most
useful for describing aquatic soundscapes. Protocols for
underwater soundscape surveys
Analyses of the contribution to sound levels from natural sources,
including biological sources
Breakdown of the overall contribution to sound levels from man-
made and other sources. Agreement on how measurements of the
outputs from different sources should be compared
Methods for comparing the contribution of different sources to
the overall aquatic soundscape, in the form of inventories or
budgets
Scientific programs that monitor trends in soundscapes through
the acquisition of long-term data sets with immediate emphasis in
areas of future change and/or critical habitat
A long-term commitment for the establishment of ocean
observing stations dedicated to ‘‘ecological’’ sound
measurements and for programs to survey different ocean
soundscapes
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decay. Near the source, the pressure rise time for high
explosives, such as TNT, is nearly instantaneous with
an exponential decay after the initial impulse. In
contrast, the impulse rise time to peak pressure with
explosives such as black powder is around a millisec-
ond (Urick 1983) and the decay of the impulse
following peak pressure is slower.
The original shock wave is thought to be the
primary cause of harm to aquatic life at a distance from
the shot point; the sound generated by the pulsating
bubble may also contribute significantly to damage
(Cole 1948). Explosions beneath the substrate may
generate seismic waves, travelling along the interface,
which may be detected by those animals with particle
motion detectors, including benthic fishes and
invertebrates.
There are several guidelines for the protection of
aquatic life during the use of explosives in water
(Young 1991; Keevin and Hempen 1997; Wright
1998). Yelverton et al. (1975) looked at the relation-
ship between fish size and their response to underwater
blasting although it is not clear whether this relation-
ship is the same for sound as it is for explosions
(Casper et al. 2013b). A literature synthesis report on
the explosive removal of offshore structures is espe-
cially informative on recommended procedures to be
followed (CSA 2004).
Seismic airguns
The airgun is the primary sound source used for
seismic exploration by the oil and gas industry.
Airguns work by producing an air bubble from a
compressed air supply (e.g., Mattsson et al. 2012; CSA
2014). The sound impulse generated by a single airgun
is omnidirectional, with greatest energy at low
frequencies, typically on the order of 20–50 Hz, with
declining energy at frequencies above 200 Hz. Arrays
consisting of several air guns are towed behind vessels
during a seismic survey. The interaction of multiple
guns fired simultaneously enhances the primary pulse
over the trailing bubble pulses and, through suitable
geometric arrangement, results in vertical focusing of
the sound energy. During the survey, the array is fired
at regular intervals (e.g., every 10–15 s), as the towing
vessel moves ahead. The sound pulse is directed
downwards to enter the seabed and the reflected sound
is detected by long hydrophone arrays streamed
behind the vessel (streamers) (Caldwell and Dragoset
2000).
The source level (a measure of the acoustic noise
output) of an airgun array is typically estimated from
measurements made some distance away and back
calculated to a specified distance from the source
(typically 1 m). The source level can vary greatly with
the design of an array and the number of airguns in the
array (Richardson et al. 1995). Most of the energy
produced is in the 10–120 Hz bandwidth (Richardson
et al. 1995), but higher frequencies do propagate
horizontally. Because the array itself is often very
large, back calculation from far field measurements is
likely to underestimate the source level.
When acoustic energy in the water encounters the
bottom, a variety of transmission modes can occur,
including both body waves (shear and longitudinal) as
well as interface waves such as head waves. The
interface waves can generate large vertical and
horizontal particle motion components within the
substrate at levels that can be detected by fishes and
perhaps invertebrates.
Impact pile driving
Impact pile driving is commonly used for the
construction of foundations for a large number of
structures including offshore wind turbines, harbor
walls, bridges, and offshore structures for the oil and
gas industry (reviewed in Popper and Hastings 2009).
The pile is a long tube, stake, or beam that is driven
into the seabed, often by means of a hydraulic
hammer. Sound is generated by direct contact of the
pile with the water as well as by shear and longitudinal
ground-borne pathways within the seabed or through
the ground if the pile is on land adjacent to water (e.g.,
Hazelwood 2012; Hazelwood and Macey 2015). The
substrate can contribute via direct propagation or
interface (Sholte-like) waves (sometimes called
ground-roll). The latter originate at the water sediment
interface and have large velocity components that
decay rapidly with vertical distance from the interface
(Brekhovskikh and Lysanov 2003). Such waves are
much more likely to affect bottom-living fishes and
invertebrates than those in the water column. Shear
waves and interface waves travel slower than com-
pression waves (sounds) and their peak energy is at
lower frequencies (Dowding 2000).
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Of particular concern are high energy impulsive
sounds generated by impact driving of large diameter
steel shell piles (Illingworth and Rodkin 2001,2007;
Reyff 2012). The impulsive sounds generated by
impact pile driving are characterized by a relatively
rapid rise time to a maximal pressure value followed
by a decay period that may include a period of
diminishing, oscillating maximal and minimal pres-
sures. The bulk of the energy in pile impact impulses is
at frequencies below 500 Hz, within the hearing range
of most fishes, with much less energy above 1 kHz
(Laughlin 2006; Rodkin and Reyff 2008). Moreover, it
is possible that the pressure levels at some distance
from the driven pile are greater than at locations closer
to the pile when sub-surface waves, generated by the
pile, re-enter the water column and combine with the
water-borne signal (Popper and Hastings 2009).
Dredging
Dredging or mining of materials from the seabed can
be conducted by mechanical means or by suction (see
National Research Council (2002) for a review of
marine dredging). Mechanical dredging involves the
use of a grab or bucket to loosen the seabed material
and raise it to the sea surface. In contrast, suction
dredging involves raising loosened material to the sea
surface by way of a pipe and centrifugal pump.
Bucket dredges produce a repetitive sequence of
sounds generated by winches, bucket impact with the
substrate, bucket closing, and bucket emptying (Dick-
erson et al. 2001; Robinson et al. 2011). Grab and
backhoe dredgers are also characterized by sharp
transients from operation of the mechanical parts.
Suction dredgers produce a combination of sounds
from relatively continuous sources including engine
and propeller noise from the operating vessel and
pumps and the sound of the drag head moving across
the substrate.
De Jong et al. (2011) reported measurements of
radiated noise from Dutch dredgers involved in the
extension to the Port of Rotterdam. Robinson et al.
(2011) carried out an extensive study of the noise
generated by a number of trailing suction hopper
dredgers during marine aggregate extraction. Source
levels of six dredging vessels were estimated and an
investigation undertaken into the origin of the radiated
noise. Source levels at frequencies below 500 Hz were
generally in line with those expected for a cargo ship
travelling at modest speed. Levels at frequencies
above 1 kHz were elevated by additional noise
generated by the aggregate extraction process. The
elevated broadband noise was dependent on the
aggregate type being extracted with gravel generating
higher noise levels than sand. There were significant
differences between source level measurements
reported by de Jong et al. (2011) and Robinson et al.
(2011), especially at high frequencies. Both reports
estimate the dipole source levels.
Very little research has been carried out on the
effects of sound from dredging on fishes and aquatic
invertebrates. In general the effects will be chronic
rather than acute. Behavioral responses and masking
effects are to be expected, with possible negative
consequences.
Operating wind farms
Sound generated by a wind farm is reported to be much
lower during the operational phase than during con-
struction (Madsen et al. 2006; Thomsen et al. 2006).
The greatest source of sound from wind farms comes
during construction when pile driving is used to lay
foundations (see above). However, whereas construc-
tion might affect marine animals for a relatively short
period of time, operational sound has the potential to
cause chronic effects over much longer periods.
The principal source of sound from an operational
wind farm is turbine noise that propagates into the
tower and foundations, coupling the sound into the
water and seabed (OSPAR 2009). Most of the noise
appears to be generated below about 700 Hz and is
dominated by narrowband tones (Wahlberg and West-
erberg 2005;Madsenetal.2006). There may also be
noise from vessels used to maintain the wind-turbines.
Sound levels within wind farms are not significantly
higher than the background noise (Nedwell et al. 2007).
The highest level noted by Wahlberg and Westerberg
(2005) was for a narrow band tone at approximately
180 Hz. There is also a particle motion component to
sounds generated by wind farms, the sound component
detected by all fishes, including sharks, and many
invertebrates (Sigray and Andersson 2012).
Vessel noise
While a complete understanding of the relative
contributions of various sources of sound in the
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marine environment is lacking, a significant portion of
human noise results from the increasing number of
large commercial ships operating over wide-ranging
geographic areas, which can result in chronic noise
exposure. Most vessels, but particularly large ships,
produce predominately low frequency sound (i.e.,
below 1 kHz) from onboard machinery, hydrody-
namic flow around the hull, and from propeller
cavitation, which is typically the dominant source of
noise (Ross 1987,1993). Radiated vessel noise relates
to many factors, including ship size, speed, load,
condition, age, and engine type (Arveson and Vendit-
tis 2000; Richardson et al. 1995; National Research
Council 2002,2003). Source levels of vessels can
range from\150 dB re: 1 lPa at 1 m to over 190 dB
for the largest commercial vessels (Scrimger and
Heitmeyer 1991; Richardson et al. 1995; Arveson and
Vendittis. 2000; Wales and Heitmeyer 2002; Hilde-
brand 2009; McKenna et al. 2012). Note that it is not
always clear whether authors are reporting estimated
source levels or received noise levels.
The number of commercial ships in the ocean has
doubled between 1965 and 2003 to nearly 100,000
large commercial vessels, and shipping industry
analysts forecast that the amount of cargo shipped
will again double or triple by 2025, with an attendant
increase in the amount of ambient noise entering the
ocean from commercial shipping (National Research
Council 2003). There may also have been a substantial
increase in sound levels in coastal waters, and in rivers
and lakes, as a result of an increase in the number of
smaller pleasure and recreational fishing vessels. One
of the most serious implications of this increase in
shipping noise is the chronic impact it may have in
terms of masking sounds of the soundscape, including
sounds of biological origin, affecting communication
in fishes and invertebrates.
Fishing
Fishing by means of towed fishing gears involves a
vessel dragging a net fitted with spreading and bottom
contact devices across the seabed. Sound is generated
both by the towing vessel and by the fishing gear being
dragged across the seabed. Chapman and Hawkins
(1969) gave early consideration to the effects of these
sounds. The greatest contribution from fishing gears
comes particularly from bottom trawls, which are
fitted with chains, rollers, and metal bobbins that
generate irregular sounds as they come in contact with
one another and with the seabed. There are also low
frequency (below 100 Hz) sounds from the vibrations
of warps or wires connecting the trawl to the ship, the
trawl doors or spreading devices, and contact with the
seabed. No published information on absolute levels
or typical spectra is currently available. In some parts
of the ocean fishing vessels operate almost continu-
ously, with possible chronic effects. There have been
no recent studies of the impact of noise from fishing
vessels, but there has been interest in reducing noise
levels from fishery research vessels in order to reduce
any impacts upon fish during stock assessment surveys
(reviewed by De Robertis et al. 2012).
Sonar
Sonar is widely used by fishing and other vessels.
Typical sonars include depth sounders, fish-finding
sonars, fishing net control sonars, side-scan sonars,
multi-beam sonars, and a variety of sonars for
mapping the topography of the seabed. The principles
of sonar operation are described by Ainslie (2010).
Sonars work at frequencies from 10 to 800 kHz.
Although ultrasonic frequencies are attenuated over
short distances by absorption, the contribution to
ambient noise is significant due to the large numbers of
such units.
Sonars are generally operated at frequencies well
above the hearing ranges of most fishes and inverte-
brates, with the exception of some clupeid fishes,
including shads and menhaden, which can detect and
respond to ultrasonic frequencies (Dunning et al.
1992; Mann et al. 1997).
Some military sonars operate at low frequencies
(1 kHz and less), or mid frequencies (1–10 kHz) that
do fall within the hearing range of fishes. The signals
projected include combinations of swept frequency
(FM) and tones pulses. As these sonars operate at large
ranges the signals can be very intense. Investigations
using low and mid-frequency naval sonars have shown
no tissue damage in fishes, although there is the
potential for temporary hearing loss in some speci-
mens of some species (Popper et al. 2007; Kane et al.
2010; Halvorsen et al. 2012c).
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Other continuous sounds
Vibratory pile driving produces a continuous sound
with peak sound pressure levels lower than those
observed in impulses generated by impact pile driving.
The principle of operation is that counter-rotating, out-
of-balance masses rotate in an enclosure attached to
the top of the pile. The rotating masses generate a
resultant vertical vibratory force that slowly forces the
pile into the substrate. Sound signals generated by
vibratory pile driving usually consist of a low funda-
mental frequency characteristic of the speed of
rotation of the revolving mass in the vibratory
hammer, typically on the order of 30 Hz, and its
higher harmonics (e.g., Laughlin 2006).
There is increasing interest in the energy generation
by wave and tidal power. Few sound measurements
are available for these devices and there have been no
scientific studies of their impact on fishes and inver-
tebrates (Table 2).
Topic 3: sound exposure metrics
An issue that arises both in describing soundscapes and
examining the sounds produced by particular sources is
how best to describe the sounds. A variety of metrics exist
for the physical description of underwater sounds (e.g.,
Ellison and Frankel 2012; Ainslie and De Jong 2015). It is
important to consider the utility of these metrics for
investigating the effects of sounds upon aquatic animals.
Table 2 Characterizing man-made sources
Drivers for information acquisition Information gaps
The nature of the sound field (spectral, temporal, and spatial)
generated by various man-made sound sources is crucial to
understanding the effects of sound exposure. There are currently
few agreed standards for measuring the output of different sound
sources. Particle motion, which is an important component of
sound detection for fishes and invertebrates, is seldom measured.
Particle motion requires vector rather than scalar measurements
There is currently no archive of sound files, recorded to an
agreed-upon standard, providing examples of the sounds
generated by different sources
Sounds of differing characteristics (e.g., impulsive vs.
continuous; short vs. long term) have different effects upon
animals. Those characteristics that are especially damaging to
fishes and invertebrates need to be defined, so that impacts might
be reduced
The oil and gas industry has conducted some research that
describes the outputs of seismic sources. Little research has been
done on other potentially damaging sources, including pile
driving where substrate borne vibration may be especially
important to fishes and invertebrates
Of considerable concern is how the output of sound sources
should be measured and the effects of different sound sources on
fishes and invertebrates assessed. Sound sources and their outputs
must be monitored and analyzed from the perspective of the
affected animals if their effects are to be fully understood
There is particularly strong interest in describing sounds
appropriately in terms of their cumulative and aggregate effects
upon aquatic animals (see Topic 5 on Effects)
What future trends should we expect in the development of sound
sources? Are aquatic animals likely to be subjected to larger pile
drivers, more extensive seismic surveys and wider swathes of
dredging and aggregate abstraction in the future as technology
develops?
Characterization of the sounds generated by different sources, in
terms of particle motion as well as sound pressure to agreed
standards using appropriate metrics and terminology
Partnership between government and industry to undertake
research on the outputs of different sound sources. A specific
example is pile driving, for which sediment transmission may be
important but the sound fields have not yet been adequately
characterized in terms of sound pressure, particle motion, and
other characteristics (rise time, degree of kurtosis etc.)
Information on the particle motion associated with interface
waves and ground roll that may affect fishes and invertebrates,
especially from pile driving and seismic sources
Characterization of impulsive sounds. What is it that makes some
sources more damaging than others? Is it the peak amplitude, the
total energy, the rise-time, the duty-cycle, or all of these features
that determines whether tissues are damaged?
Identification of the characteristics of continuous sound most
likely to have effects on animals
Determination of whether the effects on fishes and invertebrates
are similar or whether different metrics and response
characteristics are needed for different groups
Preparation of a sound archive, providing examples of sounds
generated by different sources, recorded to agreed standards
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Measurement parameters are not well defined for
underwater sounds, especially for impulsive sounds.
The Dutch research institute, TNO, recently published
a set of standards for measurement and monitoring of
underwater sound (see Ainslie 2011). The document is
intended to provide an agreed upon terminology and
conceptual definitions for use in the measurement
procedures for monitoring of underwater noise.
Measurements close to sources are often in the non-
linear portion of the sound field especially for pile
drivers and explosions and to some degree for seismic
sources. It is in these regions that damage to fishes and
invertebrates may occur.
Sound can be measured not only in terms of sound
pressure but also in terms of acoustic particle motion
(Ellison and Frankel 2012; Rogers et al. 2015). As a
vector quantity with both magnitude and direction,
particle motion is the oscillatory displacement (m),
velocity (m/s), or acceleration (m/s
2
) of fluid particles
in a sound field. Although some fishes are sensitive to
sound pressure, most fishes and invertebrates detect
particle motion (Popper and Fay 2011). It is therefore
especially important to examine the magnitudes of
both sound pressure and particle motion generated at
different locations by man-made sound sources.
With some sources, including both pile drivers and
seismic airguns, it is likely that interface waves,
consisting of large particle motions close to the
substrate (ground roll), are set up that travel at speeds
different from the speed of sound.
Particle motion may be of particular interest in
terms of its effects on fishes and invertebrates. Particle
motion may act in different directions. While there has
been great interest in the last few years in developing
vector sensors for navy applications, the technology is
not mature and measurements cannot be made
routinely. Particle motion is not a standard output
from propagation models either. A clear need is to
develop easily used and inexpensive instrumentation
and methodologies to characterize particle motion
from various sound sources, perhaps concurrent with
measures of sound pressure at the same locations
(Table 3).
Topic 4: sound propagation
As sounds travel away from the source their charac-
teristics change. Examination of the changes accom-
panying sound propagation is important for
interpreting measurements made in the field and
requires the application of models to assist in
estimating effects upon animals. While there are many
models for propagation, most of these have been
developed for use in deep water basins (oceans) and
either have to be modified or new models developed
for sound propagation in shallower waters, including
rivers, lakes and harbors. The issue with shallower
water is that there is substantial interaction of the
sound with the surface and bottom characteristics, and
this can result in differential attenuation of sounds at
Table 3 Metrics and terminology
Drivers for information acquisition Information gaps
A wide range of instruments and metrics are used to measure,
describe, and analyze underwater sounds. However, currently
sounds are only described in terms of sound pressure, whereas
many fishes and invertebrates respond to particle motion
Increasingly, biologists and others without specialist knowledge
of acoustics are conducting measurements and applying different
metrics to different taxa, often without guidance on the most
appropriate metrics
Much of the literature concerned with the effects of underwater
sound uses differing and confusing terminology. There are no
widely accepted definitions or terminology applicable to
underwater sound for universal use. Even the common term
sound pressure level is defined in different ways by ANSI and
ISO, the two main standards organizations. There is no widely
accepted definition of source level. The lack of a standard
terminology creates ambiguities in the interpretation of data and
assessment of effects
Consensus on the adoption of relevant and universally acceptable
metrics for sound pressure and particle motion so that sounds
may be described appropriately. This will enable proper
comparison of the effects of sounds of different types on different
taxa
Development of a common terminology for sound measurement
and exposure that is useful and understandable to the whole
community—from acousticians to biologists to regulators. An
authoritative and critical glossary of terms in current use is also
required
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different frequencies, with very little propagation of
sound energy at frequencies that are longer in wave-
length than the depth of the water (Rogers and Cox
1988). Many estimates made of source levels are based
on sound radiation from a point source in deep water.
Many man-made sources are deployed in shallow
water and the sources themselves are large and
distributed (for example the airgun arrays used for
seismic surveys). Some of these sources generate
seismic and interface waves within the substrate,
which must be taken into account especially for fishes
and invertebrates living close to or within the
substrate. It is important that propagation models take
these considerations into account (see Pine et al. 2013)
(Table 4).
Topic 5: effects of sound on fishes
and invertebrates
There are more than 32,000 known species of fishes
(www.fishbase.org) and far more species of aquatic
invertebrates. Research into the effects of acoustic
exposure has examined only a fraction of fishes or
invertebrates. There is an immediate need to identify
those species of greatest interest for managers and
regulators, to group those species based on common
physical or physiological characteristics, and to
determine if those common characteristics result in
common responses to acoustic exposures (see Popper
et al. 2014).
To achieve this goal, three issues will have to be
addressed. The first will be to identify the appropriate
characteristics for grouping of fishes and inverte-
brates. The second issue will be to identify appropriate
criteria for assessing the effects of sound on species
and species groups (e.g., Hawkins and Popper 2014).
The third issue is to decide how the appropriate studies
should be conducted. Can they be done in the
laboratory or do they have to be done in the field?
Methods for measuring fish hearing are highly vari-
able, with much of the variability a function of the
acoustic environment in which studies have been done
(Ladich and Fay 2013) and how the sound fields are
produced and calibrated (Rogers et al. 2015). Special
steps must be taken to ensure that aquatic animals are
exposed to sounds under carefully controlled condi-
tions in order to obtain replicable and reliable data
(Table 5).
Topic 6: sound production, sound detection
and exposure to man-made sounds—invertebrates
There are almost no data on sound detection by aquatic
invertebrates. The few experiments that have been
Table 4 Sound propagation
Drivers for information acquisition Information gaps
The propagation of sounds through the sea and seabed can
greatly influence the sound received by fishes and invertebrates.
Propagation models are available for specific oceanic
environments (i.e., shallow, deep, ice covered, and temperate
waters). However, those models have primarily been developed
by industry for their own purposes (e.g., for estimating geological
resources) and do not provide the relevant information needed for
assessing the exposure to which animals are subjected or
predicting biological effects. Researchers and regulators need to
be able to estimate the received levels of sound pressure and
particle motion to which aquatic animals are exposed in the water
column and close to the seabed. Current models have not been
designed to do that
With respect to the masking of biological sounds, there is
concern that impulsive sounds might merge with one another
over distances as a result of reverberation and other effects
Some sound sources, including seismic airguns and pile drivers,
send energy into the seabed, creating substrate vibrations that
may affect benthic fishes and invertebrates
Models of sound propagation that are specifically tailored to
estimate the exposure to which fishes and invertebrates will be
subjected, expressed in terms of sound pressure and particle
motion, for animals in the water column, close to the sea surface,
or close to the seabed
Characterization of changes in man-made sounds over large
distances from the source, particularly factors that render them
likely to mask biological sounds
Information about propagation of sound and vibration through
the seabed by means of interface waves—this is especially
relevant to benthic fishes and invertebrates
Understanding the effects over large ocean basins of multiple or
continuous activities that alter the soundscape
Characterization and modeling of sound propagation in shallower
waters
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done indicate that only low frequency sounds are
detected and that it is the particle motion component of
the sound field that is important (e.g., Mooney et al.
2010,2012; Hughes et al. 2014). There are no data that
indicate whether masking occurs in aquatic inverte-
brates. There are also only a few studies that indicate
whether man-made sounds have any impact on
invertebrate behavior. A study of the effects of seismic
exploration on shrimp, suggests no behavioral effects
from sounds with a source level of about 196 dB re 1
lPa rms at 1 m (Andriguetto-Filhoa et al. 2005). There
is, however, evidence from laboratory experiments
that metamorphosis of the megalopae of crabs is
significantly delayed when animals exposed to either
tidal turbine or sea-based wind turbine sound, com-
pared to silent control treatments (Pine et al. 2012). In
Table 5 Effects of sound on fishes and invertebrates
Drivers for information acquisition Information gaps
The great diversity of fishes and invertebrates poses major
problems in understanding the effects of sound upon them. It is
not just diversity of species within each taxonomic group but also
diversity of animal size and life history status within each
species. An important question is whether it is possible to
identify particular ‘‘types’’ of animals that may serve as models
for other species and life history stages
In considering fishes it is important that cartilaginous species
(sharks and rays) are considered along with the bony fishes
Knowledge of the hearing abilities and behavior of fishes and
invertebrates with respect to sound is not just of academic
interest. Hearing threshold curves or audiograms are already
being used in environmental statements to assess whether
animals are potentially affected by man-made sounds. Metrics for
impact assessment, and especially those based on weighted
frequency responses, require reliable measurements of hearing
abilities
The use of physiological methods to measure hearing abilities is
less satisfactory than the use of behavioral methods.
Physiological methods (e.g., auditory evoked potentials) only
measure detectable responses from the ear or lower portions of
the brain. They do not fully reflect the ability of the brain of the
animal to process and extract information, or whether there will
be a behavioral response by the animal
Information on the masking of biologically important sounds by
‘real’ sounds—including man-made sounds is critically
important
Currently, despite strong interest in determining how fishes and
invertebrates use sound and the soundscape and respond to man-
made sound, there are remarkably few experimental data. There
are almost no observations obtained from fishes and invertebrates
exposed to man-made sounds under controlled or field
conditions. Valid audiograms are only available for a handful of
species. Many studies have been carried out under inappropriate
acoustic conditions where the reliability of acoustic
measurements has been open to doubt. There is a lack of facilities
in which sound signals can be presented to fishes and
invertebrates under carefully controlled conditions. If appropriate
acoustic conditions can be provided then it should be possible to
investigate further the thresholds or criteria for the occurrence of
different effects from exposure to sound, and how they change
with different sound types and levels. It should also be possible to
determine those source characteristics that cause detrimental
effects; e.g., magnitude, rise time, duration, kurtosis, duty-cycle
Confirmation of those anatomical features (including the
presence of a swim bladder) that indicate the sensitivity of fishes
to sound and that can provide, a useful basis upon which to
categorize fishes for experimentation
Investigation of the anatomical features of invertebrates that
influence their sensitivity to sound so that representative species
can be selected for experimentation
Establish well-equipped field sites where the response of animals
can be examined under controlled acoustic conditions to extend
knowledge of hearing by fishes and invertebrates. Facilities
should provide appropriate depths and quiet ambient noise
conditions, allowing precise measurement of sound stimuli
Measures of hearing must be made, wherever possible, using
behavioral methods since physiological measures (e.g., auditory
evoked potentials) do not give an accurate indication of the
detection ability of animals
Specially designed tanks can play a role in enabling precisely
controlled and measured sound stimuli to be presented to fishes
and invertebrates
Resolution of methodological difficulties in presenting
measurable sounds to fishes and in determining thresholds to
different types of sound
Development of appropriate instrumentation to accompany these
special acoustic conditions
Experimentation under similar conditions to evaluate injury and
physiological damage to aquatic animals including assessment of
the relative importance of factors like rise-time and kurtosis, and
to assess cumulative effects, recovery from injury and other
important aspects of sound exposure
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contrast, mussel larvae showed significantly faster
settlement when exposed to the underwater noise
produced by a 125-m long steel-hulled passenger and
freight ferry (Wilkens et al. 2012). Boudreau et al.
(2009) investigated the impact of high-level impulsive
sounds on snow crabs, but showed no short or long-
term effects of seismic exposure in adult or juvenile
snow crabs or on eggs. However, Aguilar de Soto et al.
(2013) reported malformations in scallop larvae and
developmental delays resulting from exposure to
seismic airguns.
Wale et al. (2013) reported that the playback of
simulated ship noise under laboratory conditions
increases shore crabs’ metabolism. Increased metab-
olism is a sign of stress and could potentially reduce
the growth of crabs and have implications for their
survival. However, caution is needed when interpret-
ing these results in a real-world context (Table 6).
Table 6 Sound production, sound detection and exposure to man-made sounds—invertebrates
Drivers for information acquisition Information gaps
Almost nothing is known about the detection of sound and
vibration by aquatic invertebrates. Some invertebrates such as
snapping shrimp, mantis shrimp and lobsters are known to
produce specific sounds, but the role of these sounds remains to
be determined. The role of sound in lives of these animals has
hardly been explored, and information on the impact of man-
made sounds is almost totally lacking. There is a particular lack
of controlled exposure experiments on invertebrates. There have
been few studies of the potential of sound exposure to cause
mortality or sub-lethal injury in marine and coastal invertebrates.
The few studies carried out indicate a potential for sub-lethal
responses, detected using biochemical, physiological, or
histopathological measurements
In this state of ignorance there needs to be a focus on examining
those species that are of greatest interest, either because of their
ecological importance, or their role in supporting commercial
fisheries, or because sound is suspected of being important to
them. Especially important animals might include Crustaceans
(crabs, lobsters, shrimps), Mollusks (scallops, clams) and
Cephalopods (squid, octopus), and those organisms making up
the zooplankton
Having selected priority species, it would be sensible to
investigate how well they can detect sounds, and to examine how
they use sound in their everyday lives. Do some or all of these
invertebrates communicate by means of sound? Is sound
important for vital life functions like reproduction, migration,
feeding, or choice of habitat? Are the sounds important to
invertebrates likely to be suppressed or masked by man-made
sounds that alter the soundscape? How does exposure to sound
affect invertebrate physiology and their behavior? Are there
biomarkers that might indicate effects? What amplitudes of
sound and vibration potentially cause effects, and can dose/
response curves be developed?
The effects of exposure of aquatic invertebrates to man-made
sounds has been examined in only a few species, but sufficient
work has been done to indicate that there may be tissue injury
and other physiological effects from exposure to high level
sounds
There is a particular lack of knowledge on the behavior of
invertebrates in response to sound. Do any invertebrates show
substantial behavioral reactions that potentially alter fitness (e.g.,
reductions in settlement within favorable habitats, altered
reproductive behavior)?
Identification of which marine and coastal invertebrates are of
most concern with respect to exposure to man-made sound
Determination of the importance of sound to invertebrates. This
could include cataloguing the sounds they produce; their ability
to detect sounds; their vulnerability to masking or suppression of
calling following exposure to man-made sounds; whether they
engage in acoustic and other activities related to their long-term
fitness, e.g. during spawning; whether they use sound cues during
their migrations or in selecting suitable habitats
Development of better information on the ability of invertebrates
to detect sound and vibration, including:
whether invertebrates are responsive to sound pressure or
particle motion; which sound and vibration receptors are
involved and how sensitive they are;
whether high level sounds damage these receptors and/or other
tissues;
whether the receptors regenerate if they are damaged;
whether some invertebrates are especially sensitive to substrate
vibration;
whether invertebrates can distinguish between sources at
different distances or sounds from different directions;
whether they can distinguish between sounds of differing
quality;
whether sound detection by invertebrates is masked by man-
made sounds or if invertebrates can detect signals in the
presence of biological maskers; whether sound exposure can
result in hearing loss
Research on the effects on aquatic invertebrates of exposure to
man-made sounds and substrate vibrations
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Topic 7: sound production—fishes
It is still not clear how widespread sound produc-
tion is amongst fishes, although it is likely to be far
more extensive than currently known. The behavior
of fish is often suppressed under aquarium condi-
tions unless very special measures are taken to
provide a quiet environment, with similar charac-
teristics to the natural environment. Even where
particular sound-producing species have been exam-
ined, and it is evident that sound is important to
the species, it has not always been possible to
examine the full range of their acoustical behavior.
In those fishes that have been examined closely it
is evident that sound is often associated with
reproductive behavior. However, spawning behavior
of and the role of sounds in the reproductive
process have yet to be described for most fishes. It
is evident that sound production is found in a wide
range of families and species and it appears to have
evolved independently in many groups (e.g., Tavo-
lga 1971; Myrberg 1978,1981; Zelick et al. 1999;
Bass and Ladich 2008) (Table 7).
Topic 8: sound detection—fishes
Sound is important to fishes and is also likely to be
important to many aquatic invertebrates. Many fishes,
and at least some invertebrates, depend on sound to
communicate with one another, detect prey and preda-
tors, navigate from one place to another, avoid hazards,
and generally respond to the world around them.
The presentation of measured sound stimuli to
fishes under experimental conditions presents great
difficulties. The relationship between sound pres-
sure and particle velocity in the majority of
experimental tanks is extremely complex, and there
is no reliable way of calculating the relative levels
of the two quantities (Parvulescu 1964;Grayetal.
2015, Rogers et al. 2015). Both parameters should
be measured, but calibrated particle motion detec-
tors are not widely available and these measure-
ments are rarely done. Audiograms (measures of
hearing sensitivity versus frequency) and sound
pressure thresholds presented in the literature must
be treated with great skepticism unless the sound
field has been carefully specified. Relatively few
Table 7 Sound production—fishes
Drivers for information acquisition Information gaps
Some fishes make sounds that are important in their everyday
lives. Commercially important vocal fishes include the families
Gadidae (codfishes), Sciaenidae (croakers and drums), and
Serranidae (groupers)
There is considerable scope for man-made sounds to suppress or
mask those sounds with potentially deleterious effects upon vital
functions such as spawning
Identification of those fishes engaging in acoustic activities
important for their long-term fitness, such as spawning, and
finding locations where vocalizing aggregations occur
Basic research on the sounds made by fishes, and the role of
sound production in their lives, including seasonal, demographic,
situational or species differences in calling behavior
Research on the vulnerability of fishes to suppression or masking
by man-made sounds
Ability of fishes to compensate for changing noise conditions by
changing their calls
Creation of a library of sounds produced by marine and
freshwater fishes and invertebrates. Its absence hinders use of
passive acoustics as a tool for determining effects of sound on
behavior, as well as research on the role of the soundscape in fish
ecology
To support the library, there is also a need for new tools that use
multiple modalities of observation in combination with passive
acoustics to identify unknown biological sound sources and
document associated behavior. Better software tools are needed
to automate measurements of sound characteristics (such as
number, duration, and frequency of sounds, etc.) and to identify
particular sounds
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experiments on the hearing of fishes have been
carried out under appropriate acoustical conditions
and the results from many of the measurements
made in tanks, and expressed solely in terms of
sound pressure, are unreliable (Table 8).
Topic 9: masking
There is always a background level of sound in the sea,
and ambient sounds may have an impact upon the
lowest sound levels that fishes and other animals can
hear. Interference with the detection of one sound
(generally called the signal) by another sound is called
masking, and the sound that does the masking is
generally called the masker (see Fay and Megela
Simmons 1999) (Table 9).
Topic 10: effects of sound in terms of injuries
and changes in physiology
Death and injury are probably the most easily
observed and dramatic end-points in terms of
responses to sound for fishes (and invertebrates).
There are only the most limited data on mortality in
fish. There have been several reports from Caltrans
(2001) documenting fish mortality very close to pile
driving sources, and there is also confirmation that
explosions will kill nearby fish (e.g., Yelverton et al.
1975; Keevin and Hempen 1997; Govoni et al. 2003,
2008; also reviewed in Popper and Hastings 2009).
However, death has rarely been documented for
exposure to continuous sound sources. There is some
evidence from the gray literature that fish larvae and
Table 8 Sound detection—fishes
Drivers for information acquisition Information gaps
Increased knowledge of the hearing abilities of fishes is required
to assist in examining the effects of man-made sound upon them.
There is also a need to clarify whether particular species are
sensitive to sound pressure and particle motion
An immediate question is whether fishes can be sorted into
different functional hearing groups, obviating the need to
examine every species. What do we need to know to define the
main groups?
There are severe methodological difficulties to be overcome in
conducting experiments on the hearing of fishes. Many
experiments are currently being carried out under poor acoustic
conditions. The need for appropriate conditions for the
presentation and measurement of sounds in terms of both sound
pressure and particle motion has already been emphasized. There
is also a need to perform experiments on hearing against different
levels of background noise to examine any effects from masking.
There are distinct differences between the audiograms derived
using different methods. In general, those obtained from
Auditory Evoked Potentials (AEP) measurements show lower
sensitivity but wider bandwidth than those obtained from
behavioral techniques. Currently, impact assessments are being
conducted using data on the hearing abilities of fishes that has
been determined under less than optimal acoustic conditions and
which may not be truly representative of their hearing abilities in
the natural environment. Better data are required
We know that fishes can discriminate between sounds of
differing quality and can determine the direction and distance of
sound sources. It also seems likely that some can detect substrate
vibrations. The full extent of their hearing capabilities remains to
be explored. The discrimination and recognition of sounds may
be especially affected in the presence of noise
Confirmation whether fishes can be divided into categories, based
on anatomical features (such as in the ear or relationship between
ear and swim bladder) that may represent their relative sensitivity
to sound
Information obtained under carefully controlled acoustic
conditions on the sensitivity and frequency range for both sound
pressure and particle motion in different species and different life
stages. Can the hearing characteristics of fish within different
anatomical groups be described adequately by generalized
weighting functions?
Data obtained in earlier studies under inappropriate acoustical
conditions require more critical reappraisal
Studies to determine sensitivity of fishes to substrate vibrations
Studies on the ability of fishes to discriminate between sounds of
differing quality coming from different directions and distances
and how man-made sounds affect these abilities
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juveniles may be damaged by exposure to low
frequency naval sonars (Jorgensen et al. 2005) but
other investigations of the effects of impulsive pile
driving on larvae showed no effect (Bolle et al. 2012).
Additionally, exposure of fishes to very high intensity
sonars operating at frequencies below 1 kHz and from
2 to 4 kHz showed no mortality (Popper et al. 2007;
Halvorsen et al. 2012c).
The greater likelihood is that fishes and inverte-
brates will be injured by high intensity impulsive
sounds with rapid rise times, and that some of these
injuries could result in fatalities over the short term or
over a longer term if animal fitness is compromised
(Halvorsen et al. 2011,2012a,b; Casper et al. 2012a,
b,2013a,b). If an animal is injured it may be more
susceptible to infection because of open wounds or a
compromised immune system. Even if the animal is
not compromised in some way, it is possible that the
damage will result in lowered fitness, reducing the
animal’s ability to find food or making it more subject
to predation (Table 10).
Topic 11: effects of sounds upon behavior
Perhaps the most important concern is how man-made
sounds alter the general behavior of fishes and
invertebrates. It is likely that fishes and invertebrates
will respond behaviorally to man-made sounds at
much lower sound levels than would result in phys-
iological effects. Animals are likely to show behav-
ioral responses to sounds at much greater distances
from the source than those that will result in physical
injury. Changes in behavior could have population
level effects as a consequence of keeping animals
away from preferred habitats, diverting them from
migratory routes (e.g., salmon or American shad), or
interfering with reproductive behavior. Issues not only
involve the responses of the animals but also whether
habituation occurs to repeated exposure.
There have been very few studies on the behavior of
wild (unrestrained) fishes in response to sounds
(reviewed by Hawkins et al. 2014). Such studies have
been confined to only a few species and the data are
Table 9 Masking in fishes
Drivers for information acquisition Information gaps
From experiments on the masking of pure tone signals in the
presence of noise it seems likely that man-made sounds will
mask detection of the soundscape and/or biologically relevant
sounds in some (if not all) species of fish. However, data are
available for only a handful of species and additional research is
required to examine the masking of those sounds important to
fishes (their own calls, and sounds used for navigation, habitat
detection, prey and predator detection) by changes in ambient
noise. It should be possible to predict the extent of masking by
man-made sounds based on improved knowledge of hearing
capabilities of fishes and of the types of sound generated by
different sources under different conditions
The effects of masking can be of considerable significance. This
issue is not currently being given sufficient attention in the
preparation of impact assessments, where chronic effects are
often ignored. The presence of man-made sound has the potential
to inhibit or suppress vocal behavior and to interfere with the
detection of important sound cues, and may affect vital life
functions. It is important to gain a wider knowledge of the
significance of sound in fish behavior so that the population level
consequences of masking can be assessed
Periodic and intermittent sounds may affect masking if they are
merged together as a result of long distance propagation and
reverberation. The masking potential of repetitive sounds from
seismic surveys and pile driving operations has yet to be assessed
Experimental studies examining the masking of sounds of real
importance to fishes, initially focusing on species for which
sounds have been shown to play a key functional role
Development of models predicting the degree of masking of
particular sounds by different man-made sounds under varying
conditions in the sea
The masking potential of intermittent sounds from seismic
surveys and pile driving operations remains to be assessed
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Table 10 Effects of sound in terms of injuries and changes in the physiology of fishes
Drivers for information acquisition Information gaps
Little is known about the magnitude of the effects of man-made
sounds on the physiology of fishes. It is not yet clear whether
death, injury, or physiological effects only occur when fishes are
close to the sound source or whether such effects are also evident
at a distance. Instant mortality is often not of great concern since
it is seems to occur in only a small fraction of a fish population
that is closest to an intense sound source. Rather, there is interest
in sub-lethal effects and the potential for delayed mortality
There are a number of ways of assessing physiological effects,
including tissue damage (including damage to the auditory
tissues), the use of biomarkers (measures of changes in the
physiology of the animal and levels of stress hormones like
cortisol), and changes in auditory sensitivity, for example
Temporary Threshold Shift (TTS). The importance of these
measures needs to be critically assessed. Which injuries can be
regarded as potentially lethal, and which are unlikely to affect the
animal in the long term?
There may be some biomarkers that are indicative of a real and
lasting change to the physiology of the animal, affecting vital life
functions. Other biomarkers may show only transient changes.
Effects have been observed from sounds on blood proteins, blood
enzymes, blood calcium, food consumption rates, respiration
rates, growth rates and the state of the hepatopancreas (liver) in a
variety of aquatic animals. Free radical damage has also been
observed in relation to sound exposure
Is TTS an important indicator of damage? What level of hearing
loss and persistence has significant implications for behavior?
In terms of injury and tissue damage it would appear that some
fishes, and especially those possessing gas-filled swim bladders
or other cavities, might be more susceptible to damage than
others, and that the rate of equilibration with depth is important
for these fishes
The development and application of physiological trauma indices
for fish, which quantify a qualitative assessment of injuries,
ranking the physiological costs of impairment, is important as a
means for assessing the injuries to an animal. A slight change in
an enzyme or a hormonal response might not be accorded the
same status as a change in histopathology of a vital organ
An issue of great importance is the effect of intermittent
exposure. Many man-made sounds are repeated, both through
repetition of a single source and the recruitment of additional
sounds from other sources. Are there cumulative and aggregate
effects from these repeated exposures? Is there full recovery of
function after damage? Is there is a period of healing if sufficient
time passes between sound exposures?
Assessing the effects of cumulative and aggregate exposure has
implications both in terms of dose/response relationships and
more broadly in terms of designing mitigation measures
Comparison of the relative impact of exposure to different duty
cycles (patterns of presentation) also has relevance to the metrics
used to describe and measure cumulative effects from multiple
pulses from the same source
Identification of the full range of injuries or physiological effects
that may result from exposure to different sound sources and
sound levels
Identification of the most reliable indicators (particular injuries,
physiological parameters or biomarkers) of deleterious effects
from sounds, which might be incorporated into trauma indices
and applied in determining dose/response relationships
Identification of which fishes are more susceptible than others to
injury or tissue damage
Determination of the characteristics of man-made sources that
cause injury or detrimental changes in physiology; e.g.,
magnitude, rise time, duration, duty-cycle
What is the role of anatomy (e.g., the presence of the swim
bladder and other gas spaces) in producing physiological effects
and how are these effects affected by depth, size, age, season or
other factors?
Is Temporary Threshold Shift of importance when considering
effects of some or all man-made sounds? If so, how should TTS
be determined and what degree and duration of TTS is most
likely to alter behavior?
Research on the physiological effects of repeated exposure to
sound and resolution of the best metrics for expressing the
accumulation of sound energy. Is there a better descriptor than
sound exposure level (SEL), which is now expressed in two
forms: the single strike SEL or the cumulative SEL?
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often contradictory. There is a lack of information not
only for immediate effects on fish that are close to a
source but also on fish that are more distant (Table 11).
Priorities for research derived from the gap
analysis
Many information needs are listed in the Gap Analysis
but some issues of higher priority for future research
have emerged. New research in these areas would
provide better understanding of the effects of sound on
fishes and invertebrates. A list of the highest priority
research from each topic is presented below.
Describing soundscapes
Information is required on the overall contribution
made to sound levels and sound quality in aquatic
environments from all sources. These particularly
include examining baseline ambient conditions, how
they change over time and space, and how they will be
affected by additional human activities.
There is a need to develop scientific programs that
monitor trends in soundscapes through the acquisition
of long-term data sets. It is especially important to
begin the monitoring of soundscapes in areas of future
change and/or critical habitat. At least 30 global sites
or networks are routinely collecting data on ocean
Table 11 Effects of sounds upon the behavior of fishes
Drivers for information acquisition Information gaps
The potential impact of man-made sounds extends well beyond
the distances at which physical or physiological effects occur. A
major concern is whether these sounds affect behavior, in turn
affecting vital functions such as reproduction, migrations or
choice of habitat. Behavioral impacts may range from small (and
inconsequential) awareness of sounds to fishes changing their
migratory routes, leaving favored sites for feeding and/or
breeding, or failing to detect appropriate high-quality habitat
Experiments on captive fishes, whether in tanks in the laboratory
or cages in the sea are unlikely to yield valid results. Fishes show
changes in behavior and restrictions in their behavioral repertoire
in captivity. Currently we have only poor knowledge of
behavioral responses in the wild and how they change with
different types and levels of sound. Moreover, impacts from man-
made sound on fishes leading to changed behavior must be
understood in a species specific, size specific, biological state
specific and seasonal context
Different types of sound source may elicit different behavioral
reactions or result in onset of behavioral reactions at different
sound levels. Responses may vary greatly by species, motivation
of animals, and other behavioral and physiological conditions. An
important question is whether an observed response results in
impaired access to essential habitat for feeding, reproduction,
concealment, territoriality, communication, or other life processes
It is important to consider which aspects of a sound are
responsible for a given behavioral response (i.e., exposure level,
peak pressure, or frequency content). The effects of chronic
exposure over long periods to low level sounds may be as
important as exposure to isolated high-level sounds
It is known that fishes may change their behavioral responses
after the repeated presentation of sounds. In some cases their
reactions may diminish and they may eventually ignore the
sound. The full response may be restored after an interval without
sound. There is currently little information on the occurrence of
habituation
Detailed data on behavioral responses of free-swimming fish in
their natural habitats following exposure to relevant sounds
Dose/response curves for behavioral responses to sound
exposure
Data to support ranking the significance of different behavioral
responses for a given species. The ability to distinguish between
inconsequential responses and responses that will affect vital
functions is important for defining dose/response relationships
for behavior
Examination of the effects of chronic exposure over long periods
to low-level sound
Examination of the role of habituation in behavioral responses
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noise, but in almost all cases the monitoring stations
involved have been established to perform specific
functions. A variety of sensor designs and data
collection and transmission protocols have been
applied. Many other isolated measurements of ocean
noise have been made in the course of specific studies
for military purposes or for the preparation of envi-
ronmental statements. However, there is no central
repository for these data, nor are there any standards or
protocols for data collection.
A long-term commitment is required for the
establishment of sound monitoring stations and to
programs to survey different underwater soundscapes.
Priority locations for observing stations include areas
where activities are anticipated in the foreseeable
future such as areas for energy development, con-
struction work, including roads and bridges close to
freshwater sites, and marine mineral extraction. An
important question is how much man-made sound the
environment can tolerate without its ecological status
being changed.
There is a need for a library of sounds produced by
fishes and invertebrates. Lack of such a library hinders
use of passive acoustics as a tool for determining
effects of sound on behavior and examining masking
of communication by man-made sounds.
New tools are required to identify unknown
biological sound sources and document associated
behaviors. Better software tools are also needed to
automate measurements of sound characteristics.
In addition to reporting real-time measurements of
underwater sound, monitoring stations should be
capable of collecting and storing raw data at sufficient
frequency and duration to adequately describe sound
levels at various temporal scales. Storage of raw data
enables a time series of measurements to be calculated
at a later time in different metrics, for either comparing
results to other studies or to comply with regulatory
thresholds.
Maps of the sound metrics and their statistics
collected by long-term studies using passive acoustic
monitoring networks may provide useful information
for marine spatial planning, site evaluation, and
impact assessments. Because soundscapes vary at
different locales within the regions of concern, site-
specific studies of passive acoustic monitoring should
be performed before, during, and after sound-gener-
ating activities related to the energy industry (e.g., site
evaluations using seismic air guns, construction and
operation of a energy production site).
Impacts of particular sound sources
What are the main characteristics of the sound fields
generated by human activities; expressed in terms
that will enable their effects upon aquatic organisms
to be assessed?
Information is required on the characteristics of the
sounds generated by different sources. Some sound
sources, and in particular pile drivers, where trans-
mission through the substrate may be important, have
not yet been adequately characterized in terms of the
sound fields and other disturbances that they produce.
In addition, those characteristics of man-made
sources that cause detrimental effects on animals need
to be defined. Better knowledge of the propagation of
sounds (in terms of both sound pressure and particle
motion) is required, especially for those sounds
relevant to fishes and invertebrates. There is a
particular need to investigate the propagation of sound
and vibration through the seabed, as this is especially
relevant to benthic fishes and invertebrates and for
exposure to both pile driving and seismic airguns.
There is a need to describe and fully evaluate the
effects of the sound fields (in both the near field and far
field) produced by explosions, seismic airguns, pile
driving, dredging, wind farm operation, vessel noise,
fishing activities, and sonar systems. Some research
has already been performed by the oil and gas industry
to characterize the sound fields generated by seismic
airguns and that work should serve as an example for
other industries to follow. Research related to the
impacts of vessel noise, fishing, activities, and sonar
also needs to be advanced.
Sound fields should be expressed in terms of metrics
that may be most useful in describing effects upon
marine organisms Ainslie and De Jong (2015). As many
fishes and invertebrates are sensitive to particle motion,
rather than sound pressure, it is especially important to
monitor particle motion along with sound pressure. The
development of instrumentation and software for this
purpose should receive a high priority.
Studies should provide raw data to allow for
different metrics to be applied subsequently, particu-
larly if a standard terminology is later established.
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Effects of man-made sounds on marine animals
What effects do man-made sounds have upon fishes
and invertebrates?
More information is required on the effects of sound
on fishes and invertebrates, especially in terms of
changes to their survival and reproductive success.
Experiments are required to evaluate the levels of
injury and physiological damage that are experienced
by aquatic animals as a result of exposure to sound,
including assessment of the relative importance of
acoustical factors like frequency, rise-time, and duty
cycle.
Such studies may be performed under controlled
laboratory conditions or under field conditions (e.g.,
cages, pens) but in either case the experiments must
include careful measurements of sound pressure and
particle motion received by the animal. There is a need
to develop a broader understanding of any injuries
and/or physiological effects that result from exposure
to different sound sources, sound levels, repetition
rates, and number of events. Are there particular
injuries, physiological parameters or biomarkers that
might provide evidence of deleterious effects from
sounds, and which might be incorporated into trauma
indices and applied in determining dose/response
relationships?
Assessment of effects has to include both cumula-
tive and aggregate effects of sound exposure. The
effects of repeated exposure to single and multiple
stressors and interactions between multiple stressors
(both natural and anthropogenic) must be considered.
There is a need to decide which metrics are most
appropriate for expressing the accumulation of sound
energy. This requires further information on the
degree and types of injury caused by sounds of
differing characteristics.
Key components of experimental research for
advancing our knowledge of effects of man-made
sounds on fishes and invertebrates are: (1) laboratory
or field experiments with adequate controls; (2) animal
subjects representative of the different groups defined
by sound detection ability, anatomy, ecological asso-
ciations, commercial importance, and conservation
status; (3) treatment groups exposed to sound stimuli
over different temporal scales, and either over differ-
ent spatial scales from the source or simulated levels
and characteristics sufficient to quantify mortality,
physiological damage, temporary threshold shift,
masking, and behavioral responses; (4) appropriate
instrumentation to precisely measure a suite of sound
characteristics (e.g., spectral density, sound exposure
level (single strike and cumulative), rms sound
pressure levels, measures of peakiness, rise time,
particle motion, etc.) presented to treatment groups;
and (5) processed and raw data should be adequately
archived.
More extensive and detailed knowledge of the
hearing abilities of fishes and invertebrates is required.
Hearing threshold curves (audiograms) are being used
in environmental impact assessments and/or in the
preparation of weighting curves to assess whether
animals are potentially affected by man-made sounds.
Much of the current data do not give an accurate
indication of the detection ability of the animals since
they were obtained either under unsatisfactory acous-
tic conditions or by means of physiological measure-
ments (Ladich and Fay 2013; Gray et al. 2015; Rogers
et al. 2015; Sisneros et al. 2015). Audiograms should
be developed using behavioral analysis in carefully
designed experiments that can adequately replicate the
sound characteristics of man-made sound sources
(e.g., pile driving, dredging, seismic airguns, etc.)
under ‘‘free-field’’ or ‘‘far-field’’ acoustic conditions.
Well-equipped field sites, where the response of
animals can be examined under approximate ‘free-
field’ acoustic conditions, are required to extend
knowledge of the hearing by fishes and invertebrates.
Conditions are required where animals can be exam-
ined at appropriate depths, under quiet ambient noise
conditions, and where sound stimuli can be precisely
measured. Specially designed tanks can also play a
role in enabling precisely controlled and measured
sound stimuli to be presented to fishes and inverte-
brates so that their detection abilities can be deter-
mined (Rogers et al. 2015; Slabbekoorn 2015). At the
same time, there are instances, such as with larval
fishes where behavioral methods have not yet always
been worked out, and where other approaches, such as
auditory brainstem response might provide important
data (e.g., Wright et al. 2011).
The susceptibility of animal hearing to masking by
man-made sounds especially needs to be investigated
(Dooling and Blumenrath 2015). The consequences
for fishes and invertebrates of changes to the sound-
scape need to be assessed in terms of the effects this
will have on their ability to detect sounds.
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Information on the behavioral responses of fishes
and invertebrates to different sound sources is also
needed in order to assess the effects of man-made
sounds. Information is required on responses over time
(for example to repeated exposure) and over long
distances. How do animals respond when they
encounter a sound? Do they leave an area? Do they
return later? Is their fitness impaired? Experiments
exploiting new technologies (e.g., active acoustics,
tagging) at an appropriate scale and for a variety of
sound sources should be encouraged. It is important to
note that such studies cannot be carried out in the
laboratory or even in large cages, but require detailed
observations on the behavior of animals in the natural
environment.
More information is required on the effects of
man-made sounds on the distribution of fishes and
their capture by different fishing gears. There may be
different effects on different species, on different
fishing grounds and habitat types. Access to fisheries
statistics at fine spatial and temporal scales may
provide useful insight, but fishery-independent sur-
veys using multiple gear types following before-
after-control-impact study design may provide better
information on the effects of particular man-made
sounds to catch rates and distributions (vertical and
horizontal) of fishes and commercially important
invertebrates.
Selection of appropriate species for further study
must be made carefully. Although endangered and
threatened species in areas likely to be affected by
various sound sources are of greatest interest, practi-
cally-speaking these species are often not readily
available for experimentation. In some cases it may be
necessary to examine closely related species as
surrogates. Species that are representative of the
various anatomical and ecological associations should
receive high priority for examination. Fishes could be
grouped by their swim bladder morphology and life
stage (eggs, larvae, juvenile, adult) so that emphasis
can be placed on those categories for which sound is
likely to be especially important (Popper et al. 2014;
Hawkins and Popper 2014). Invertebrates selected for
study should represent the major taxonomic groups
and those species of greatest commercial and ecolog-
ical importance should be prioritized such as bivalves
(e.g., scallops, clams), cephalopods (e.g., squid),
crustaceans (e.g., lobsters, shrimps), echinoderms
(e.g., sea urchin), and corals (e.g., coral larvae). Fishes
and invertebrates of high commercial importance (top
ten in landings or value) should also be considered.
Mitigation of effects
Can mitigation measures reduce sound exposure
and reduce and/or eliminate detrimental effects
from sound-generating activities?
Although the preceding Gap Analysis did not specif-
ically consider the mitigation of any effects this is an
important aspect of environmental impact assessment
that requires consideration. There are two kinds of
mitigation. The first involves the use of biological
information to minimize effects. The second involves
changes to the sound source to minimize effects.
To facilitate biological forms of mitigation, infor-
mation is required on those periods in the lives of
marine fishes and invertebrates, or those critical
locations, when they might be especially affected by
exposure to man-made sound. Specific requirements
are to identify critical habitats, migration routes, and
reproductive periods so that exposure might be
avoided. Such information requires close cooperation
with fisheries biologists.
For some sources there may be potentially useful
mitigation measures applied to the source itself that
might decrease the exposure of fishes and inverte-
brates to sound. Research is needed to establish the
means for reducing unwanted and damaging sound
from a range of sound sources. Industry must look
closely at making changes to those sources or seeking
alternatives to them that will cause less harm. Sound
shielding technologies capable of effectively and
verifiably reducing harm from existing sources should
also be investigated. In considering source mitigation
it is important to examine those characteristics of the
sounds that might make them especially likely to be
harmful to fishes and invertebrates (in terms of level,
duration, rise time, duty cycle etc.).
Studies are especially required to examine the
efficacy of ramp-up, soft-start and other aversive
techniques. Can fishes and invertebrates be induced to
move away from an area by using ramp up in order to
allow potentially damaging sounds to be produced
subsequently?
Passive Acoustic Monitoring (PAM) systems are
routinely used to detect marine mammals by register-
ing their natural calls. PAM systems have not yet been
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developed to detect the presence of fishes and
invertebrates, perhaps because there are fewer vocal
species and the calls are often much lower in
amplitude than those of marine mammals, making it
harder to detect fishes and invertebrates. There is a
possibility that active acoustic monitoring, by means
of sonar, may detect the presence of some fishes and
invertebrates without disturbing them. The application
of active acoustic monitoring should be further
explored.
Where mitigation measures have been imple-
mented to overcome or reduce the effects of exposure
to sound, the efficacy of those measures should be
monitored and assessed.
Measurement and description of sounds
and the conduct of acoustic experiments
It is especially important to describe sounds properly,
and conduct experiments under controlled acoustic
conditions
Agencies must come to a consensus on the adoption of
relevant and universally acceptable metrics that
describe sounds appropriately and enable comparison
of the effects of sounds of different types on different
taxa. This has to be done for both sound pressure and
particle motion.
A common terminology needs to be developed for
sound measurement and exposure that is useful and
understandable to the whole community—from acous-
ticians to biologists to regulators.
Inexpensive instrumentation, which does not
require specialist skills, is required for the measure-
ment of underwater sound, both in the laboratory and
in the ocean. Measurement of particle motion is a
particular priority.
Special acoustic facilities are required that will
enable investigators to present sounds to aquatic
animals in the laboratory, or in the field, with full
specification of the signals presented both in terms of
sound pressure and particle motion. Such field sites are
required to extend knowledge of the hearing by fishes
and invertebrates, as well as their behavioral
responses.
Acknowledgments This review is partially derived, with
permission, from a report to the Bureau of Ocean Energy
Management (Normandeau 2012) prepared by the authors. The
report, in turn, derives from and builds on a meeting on ‘‘Effects
of Noise on Fish, Fisheries, and Invertebrates in the U.S.
Atlantic and Arctic from Energy Industry Sound-Generating
Activities’’ that was initiated and funded under contract
M11PC00031 by the Bureau of Ocean Energy Management
(BOEM) Environmental Studies Program of the U.S.
Department of the Interior. We thank Kimberly Skrupky and
the many others at BOEM for their guidance and active support
for the meeting. Normandeau Associates led the BOEM project
and while working on the whole project we benefitted greatly
from collaboration with Dr. Christopher Gurshin of
Normandeau. We have learned much from discussions and
collaborations with numerous colleagues. We are reluctant to
name individuals for fear of leaving out some people, and
instead offer our greatest respect and gratitude to all of our
colleagues. Since 2007 we have had a multi-year collaboration
with a particular group of colleagues in developing guidelines
for effects of noise on fish and turtles (Popper et al. 2014). Those
individuals had a substantial impact upon our thinking. We want
to thank Kim Skrupky, Arie Kaller, and Sally Valdes for review
and comments on this revised MS. Finally, while this paper is a
synthesis and distillation of many parts of the Gap Analysis from
the BOEM report, we have also modified the analysis and
brought in new ideas and views. We take full responsibility for
any errors or omissions.
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... As with acoustic noise, the effects of vibrational noise upon a terrestrial or aquatic animal depend upon the properties of the source itself (which influence, e.g., the intensity level, duration, repetition, spectral range of emitted vibrations; see summary Box 6.2), the levels received, the background levels of vibration, and the detection abilities of the receiver (Chapman and Hawkins 1973;Tasker et al. 2010;Hawkins and Popper 2014;Hawkins et al. 2014a). As such, testing for potential effects of anthropogenic vibration can be a challenge, given the complexity of anthropogenic sources and the scenario specificity of each occurrence and the difficulties of replicating them accurately with a wider applicability. ...
... 1. Lack of available biological and experimental information on which to base mitigation continues to challenge us because of the abundant variation in living things, even within a species, e.g., behavior varies with size, physiology, individual, age, species, context, environmental parameters, and motivation (Ellison et al. 2011;Hawkins and Popper 2012;Hawkins et al. 2014a;Miller et al. 2016). 2. Impacts of vibrational noise vary with, for example, background intensity levels, propagation conditions, and the noise properties at the source (intensity level, frequency composition, duration, and repetition rate) (Kastelein 2008;Götz et al. 2009). ...
... For example, further from the source we would expect not only a decrease in noise amplitude, but also an increase in rise time, making a more gradual onset. One or both factors could play a role in how these animals respond to this acoustic stressor 28 . Yet, this result underscores the importance of taking into account the type of exposure signal when assessing impact studies on marine animals. ...
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... Human activities on, in, and near the water introduce potentially adverse sounds into the fi sh habitat. These humanmade (Anthropogenic) sounds may be audible to fi shes and they can potentially disturb or deter the fi shes, or mask other sounds that are relevant to the animals Exposure to man-made sounds can also have physiological and behavioral effects that may be detrimental to the animals [29,31,32]. Some of these human-made sounds can kill or injure fi shes and other aquatic animals, also impairing their hearing and altering their behavior. ...
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This paper describes how fish can be located using sound, especially in the sea, but also in rivers and lakes. It describes the use of sound detections, including both passive and active acoustics, and it reviews each of these technologies and shows how they can be used to understand the distribution of sound-producing species and to examine information on the spawning habitats of fishes, and their spawning behavior, and also their movement patterns. Sounds generated by humans can have detrimental effects upon fishes, and some stocks of fishes are exploited close to their safe biological limits, requiring restrictions upon those human activities that may harm them. There is a need to regulate those human activities that have adverse effects on fish.
... comm.). Less is known on the effect of anthropogenic sound on deep-sea fish (Bolgan et al., 2020), however it can disturb their communication and orientation (Hawkins et al., 2015). Raw abundances and densities of fauna may have to be adjusted to account for this type of effect, as shown in the case of strong swimmers such as sablefish, with methodologies similar to the ones applied for the estimation of true densities in baited camera experiments (Priede and Merrett, 1996). ...
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Scientific, industrial and societal needs call urgently for the development and establishment of intelligent, cost-effective and ecologically sustainable monitoring protocols and robotic platforms for the continuous exploration of marine ecosystems. Internet Operated Vehicles (IOVs) such as crawlers, provide a versatile alternative to conventional observing and sampling tools, being tele-operated, (semi-) permanent mobile platforms capable of operating on the deep and coastal seafloor. Here we present outstanding observations made by the crawler “Wally” in the last decade at the Barkley Canyon (BC, Canada, NE Pacific) methane hydrates site, as a part of the NEPTUNE cabled observatory. The crawler followed the evolution of microhabitats formed on and around biotic and/or abiotic structural features of the site (e.g., a field of egg towers of buccinid snails, and a colonized boulder). Furthermore, episodic events of fresh biomass input were observed (i.e., the mass transport of large gelatinous particles, the scavenging of a dead jellyfish and the arrival of macroalgae from shallower depths). Moreover, we report numerous faunal behaviors (i.e., sablefish rheo- and phototaxis, the behavioral reactions and swimming or resting patterns of further fish species, encounters with octopuses and various crab intra- and interspecific interactions). We report on the observed animal reactions to both natural and artificial stimuli (i.e., crawler’s movement and crawler light systems). These diverse observations showcase different capabilities of the crawler as a modern robotic monitoring platform for marine science and offshore industry. Its long deployments and mobility enable its efficiency in combining the repeatability of long-term studies with the versatility to opportunistically observe rarely seen incidents when they occur, as highlighted here. Finally, we critically assess the empirically recorded ecological footprint and the potential impacts of crawler operations on the benthic ecosystem of the Barkley Canyon hydrates site, together with potential solutions to mitigate them into the future.
... During operation, turbines introduce mechanical noise from gears, generators, hydraulic systems, and rotor blades (Lindeboom et al., 2011). Noise levels from OWFs in production are lower than those emitted by pile driving during construction, and not significantly higher than background levels (Nedwell et al., 2007) but are long-term (Hawkins et al., 2014). Most noise emitted by operational offshore wind turbines is low frequency (<1000 Hz) and is detectable by sound sensitive fish and invertebrates over several kilometres (Andersson et al., 2011;Hawkins and Popper, 2017). ...
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Offshore wind infrastructure modifies benthic habitats, affecting ecosystem services. A natural capital approach allows risks to nature-based assets and ecosystem benefits to be assessed. The UK Natural Capital Committee produced guidance for conducting natural capital assessments to aid decision making processes. Development of an asset register and risk register are key components of this methodology. The former provides an inventory of NC stocks, and the latter considers the likelihood of changes and the scale of their impact on delivery of ecosystem services. In this study, suitability of the methodology in a marine environment context was critically evaluated. Natural capital stocks before and after installation of Greater Gabbard offshore wind farm were compared and risks to delivery of ecosystem services were assessed. It was demonstrated that incorporating an assessment of impacts on natural capital assets in planning and management decisions (as an extension to traditional environmental impact assessment approaches) could further facilitate sustainable use of marine ecosystems. For example, by preventing access to bottom-trawl fisheries activities, wind farms may promote recovery and increase value of seabed natural capital assets. By also introducing aquaculture systems loss of food provision (from reduced fishing activity) could be offset whilst allowing benthic natural capital assets to recover. Natural capital assessment is relevant to the marine context. However, application of the Natural Capital Committee’s methodology was constrained by the limited coverage of standard benthic sampling tools. Given the scale of wind energy plans across the marine environment it is recommended that these shortcomings are appropriately addressed.
... The considerable breadth of these factors that may contribute to higher or lower vulnerability to harm from exposure to aquatic noise reinforce the need to address the persistent knowledge gaps that impair our ability to understand and ameliorate impacts of aquatic noise (Hawkins et al., 2015). Of particular interest here is life-history stage, which has been poorly understood relative to its importance for marine invertebrates. ...
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Anthropogenic aquatic noise is recognised as an environmental pollutant with the potential to negatively affect marine organisms. Seismic surveys, used to explore subseafloor oil reserves, are a common source of aquatic noise that have garnered attention due to their intense low frequency inputs and their frequent spatial overlap with coastal fisheries. Commercially important Southern Rock Lobster (Jasus edwardsii) adults have previously shown sensitivity to signals from a single seismic air gun. Here, the sensitivity of J. edwardsii juveniles and puerulus to the signals of a full-scale seismic survey were evaluated to determine if early developmental stages were affected similarly to adults, and the range of impact. To quantify impact, lobster mortality rates, dorsoventral righting reflex and progression through moult cycle were evaluated following exposure. Exposure did not result in mortality in either developmental stage, however, air gun signals caused righting impairment to at least 500 m in lobsters sampled immediately following exposure, as had previously been reported in adults with corresponding sensory system damage following exposure. Impairment resulting from close range (0 m) exposure appeared to be persistent, as previously reported in adults, whereas juveniles exposed at a more distant range (500 m) showed recovery, indicating that exposure at a range of 500 m may not cause lasting impairment to righting. Intermoult duration was (time between moults) significantly increased in juveniles exposed at 0 m from the source, indicating the potential for slowed development, growth, and physiological stress. These results demonstrate that exposure to seismic air gun signals have the potential to negatively impact early life history stages of Southern Rock Lobsters. The similarity of both the impacts and the sound exposure levels observed here compared to previous exposure using a single air gun offer validation for the approach, which opens the potential for accessible field-based experimental work into the impact of seismic surveys on marine invertebrates.
... Impact studies are also few (Mueller-Blenkle et al., 2010;Magnhagen et al., 2017). This knowledge gap was identified in reviews and guideline papers and relates both to impact studies as well as sound source characteristics (Popper et al., 2014;Hawkins et al., 2015;Nedelec et al., 2016;Nedelec et al., 2021). ...
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Measurement of particle motion from an offshore piling event in the North was conducted to determine noise levels. For this purpose, a bespoken sensor was developed that was both autonomous and sensitive up to 2 kHz. The measurement was undertaken both for unmitigated and mitigated piling. Three different types of mitigation techniques were employed. The acceleration zero-to-peak values and the acceleration exposure levels were determined. The results show that inferred mitigation techniques reduce the levels significantly as well as decreases the power content of higher frequencies. These results suggest that mitigation has an effect and will reduce the effect ranges of impact on marine species.
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