JNCC guidelines for minimising the risk of injury and disturbance to marine mammals
from seismic surveys: We can do better
Andrew J. Wright
⁎, A. Mel Cosentino
Department of Environmental Science and Policy, George Mason University, 4400 UniversityDrive, Fairfax, VA 22030, USA
Wild Earth Foundation,Av de las Ballenas 9500, Puerto Pirámides, Península Valdés, Chubut, Argentina
Received 10 January 2015
Received in revised form 30 August 2015
Accepted 31 August 2015
Available online xxxx
Seismic survey guidelines
The U.K.’s Joint Nature Conservation Committee 1998 guidelines for minimising acoustic impacts from seismic
surveys on marine mammals were the ﬁrst of their kind. Covering both planning and operations, they included
various measures for reducing the potential for damaging hearing –an appropriate focus at the time. Since
introduction, the guidelines have been criticised for, among other things: the arbitrarily-sized safety zones; the
lack of shut-down provisions; the use of mitigation measures that introduce more noise into the environment
(e.g., soft-starts); inadequate observer training; and the lack of standardised data collection protocols. Despite
the concerns, the guidelines have remained largely unchanged. Moreover, increasing scientiﬁc recognition of
the scope and magnitude of non-injurious impacts of sound on marine life has become much more widespread
since the last revisions in 2010. Accordingly, here we present feasible and realistic recommendations for such
improvements, in light of the current state of knowledge.
© 2015 Elsevier Ltd. All rights reserved.
Man-made noise has the potential to impact marine mammals and
other species by disrupting essential behaviours, such as communica-
tion and foraging (e.g., Hildebrand, 2005; Jasny et al., 2005; Nowacek
et al., 2007; NRC, 1994, 2000, 2003, 2005; Richardson et al., 1995;
Southall et al., 2007; U.S. Marine Mammal Commission, MMC, 2007;
Weilgart, 2007). One of the most regulated sources of noise is the seis-
mic survey conducted by the oil and gas industry and (to a much lesser
extent) geological surveys (see Simmonds et al., 2014). These surveys
employ airguns that produce sharp, loud sounds that cannot be precise-
ly controlled and include energy at frequencies as high as 22 kHz,
(e.g., Goold and Coates, 2006; Goold and Fish, 1998; Hermannsen
et al., 2015). The majority of the noiseenergy, however, isat frequencies
below 100 or 200 Hz (Goold and Fish, 1998; Hermannsen et al., 2015)
that may propagate over distances as large as 4,000 km (e.g., Nieukirk
et al., 2004, 2012) and are used heavily by baleen whales in their own
sounds (e.g., Nieukirk et al., 2004; Stafford et al., 1999). While lower fre-
quencies are functional for the surveys (e.g., below 200Hz; OGP and
IAGC, 2008), the noise at higher frequencies is unnecessary.
As of 2013 there were 142 seismic survey vessels worldwide, with
increases likely in numbers and capacity-per-vessel (Kliewer, 2013). A
large proportion of these vessels will be simultaneously active on
surveys that may persist for months and extend over huge areas (e.g.
35,000-70,000 sq. km; Clark and Gagnon, 2006). As a result, these typi-
cally coastal surveys can be detected above natural background noise
levels on 80-95 % of days at some locations on the Mid-Atlantic Ridge
(Nieukirk et al., 2012). The cumulative exposure of these surveys for
marine life collectively is enormous.
Exposure to seismic survey sounds can lead to avoidance, startle re-
sponses, vocalisation changes, and the alteration of dive and respiration
patterns (e.g., Gordon et al., 2004). However, airgun exposures can also
lead directly to temporary or permanent threshold shift (TTS or PTS; see
Southall et al., 2007). PTS has often, but perhaps not appropriately, been
used to deﬁne the onset of ‘injury’by managers (see Southall et al., 2007
and Tougaard et al., 2014).
To address these issues, the Joint Nature Conservation Committee
(JNCC) became the ﬁrst regulatory body in the world to issue guidelines
for minimising impacts of noise from seismic surveys on marine mam-
mals (JNCC, 1998). However, the “mitigation measures recommended
in the existing guidelines are more relevant to the prevention of injury
rather than disturbance”(JNCC, 2010). This focus ran contrary to the
fact that the guidelines are titled, “Guidelines for Minimising Acoustic
Disturbance to Marine Mammals from Seismic Surveys”(emphasis
added). Nevertheless, these guidelines, which became statutory in the
UK in 2001, ﬁlled a policy vacuum and have since been adopted, in
whole or in part, by several other management agencies around the
world (e.g., Brazil, Aruba, Suriname: Compton et al., 2008; Mama CoCo
SEA Project, 2015; also voluntarily used by industry in areas without
guidelines; Weir and Dolman, 2007). Any company that wishes to
conduct seismic surveys in UK continental shelf (UKCS) waters must
Marine Pollution Bulletin xxx (2015) xxx–xxx
E-mail address: firstname.lastname@example.org (A.J. Wright).
MPB-07151; No of Pages 9
0025-326X/© 2015 Elsevier Ltd. All rights reserved.
Contents lists available at ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
Please cite this article as: Wright, A.J., Cosentino, A.M., JNCC guidelines for minimising the risk of injury and disturbance to marine mammals from
seismic surveys: We can do better, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.08.045
apply for consent from the Department of Energy and Climate Change
(DECC), with adherence to the guidelines being a standard condition.
Mitigation measures required by the 1998 JNCC guidelines were lim-
ited and, despite reﬁnements, remain largely unchanged (JNCC, 2010).
For example, the training required of visual observers has become
formalised into a JNCC-approved course; and more in-depth discussions
of PAM and ramp-ups were included. However, the most notable
addition was the recognition that visual observers need to be fresh to
be effective, with advice that “two marine mammal observers should
be used when daylight hours exceed approximately 12 hours per
day…or the survey is in an area considered particularly important
for marine mammals.”However, despite wide acknowledgement
of the limitations of the JNCC guidelines and mitigation measures
(e.g., Barlow and Gisiner, 2006; Lubchenco, 2010; Nowacek et al.,
2013; Parente and de Araújo, 2011; Parsons et al., 2009; U.K.
Department of Trade and Industry, DTI, 2002; Weir and Dolman,
2007), there is still no requirement to cease operations (or ‘shutdown’)
should marine mammals be detected within the mitigation zone during
operation (JNCC, 2010). Here we re-assess the merits of the JNCC guide-
lines in light of the current state of knowledge.
2. Planning stages
Adequate planning is critical to reduce or eliminate the impact on
marine mammals. Environmental considerations throughout the
lifecycle of the project should be included in the planning process as
early as possible to facilitate informed decision-making about the best
locations for seismic activities (e.g., Nowacek et al., 2013). Avoidance
of areas where marine mammals are known to occur should be
prioritised, but if it is ultimately not possible, efforts should be made
to avoid surveys at times of particular importance, such as breeding
periods. Identifying hotspots of marine mammal abundance and those
periods when animals are particularly sensitive, however, requires
‘baseline’data. Both abundance and habitat use are subject to inter-
annual variability, thus a pre-activity record of three or more years in
length is preferable. Additionally, planning should be made for a gradual
phase-in of an activity in situations or locations when the impacts
are especially uncertain, which would inform management prior to
escalation at each step.
While the JNCC guidelines have always referred to the need for
adequate planning, they have typically fallen short of these goals.
For example, the 1998 version (JNCC, 1998) simply stated that seis-
mic surveys projects should, at the planning stages: discuss the
merits of the design of any monitoring programs; plan the timing
of their surveys to reduce the likelihood of encounters with marine
mammals; seek to reduce the unnecessary high frequency noise;
and, in areas of importance to marine mammals (as was to be deter-
mined “in consultation with the JNCC”) seek to provide the most
appropriately qualiﬁed and experienced personnel to act as marine
mammal observers (MMOs) on board the seismic survey vessel
(preferably experienced cetacean biologists, but at a minimum it was
“recommended that observers should have attended an appropriate
The 2010 version of these guidelines (JNCC, 2010) added to the
planning stages a requirement to use the lowest practicable power
levels necessary to achieve the survey objectives. However, even
here there is no speciﬁc mention of complete avoidance of particu-
larly important areas, although it could be argued that this might
be covered by the additional precautions that JNCC can impose on
a case-by-case basis. (It should also be noted, however, that advice
regarding wider risk assessments are present in the joint JNCC,
Natural England and Countryside Council for Wales guidelines for
the Protection of Marine European Protected Species from Injury
and Disturbance, although these seemingly remain in draft form:
JNCC et al., 2010).
3. Mitigation measures
The JNCC guidelines include a number of mitigation measures
designed to reduce the impact of seismic surveys on marine mammals.
However, they essentially condense down to two basic elements: main-
tenance of a pre-survey safety zone and mitigation sources.
3.1. Safety zones: size and function
While manyguidelines aroundthe world have implemented a safety
zone throughout the duration of a seismic survey (e.g., Kyhn et al.,
2011), the JNCC guidelines only require the maintenance of a pre-
survey mitigation zone (JNCC, 2010). An area of 500m radius from the
centre of the airgun array must be scanned for 30 min before the
commencement of the soft-start and determined to be clear of marine
mammals (see below). In waters deeper than 200 m the duration of
the pre-survey visual scan is extended to 60 minutes to account for
long, deep diving species (JNCC, 2010). If any marine mammal is detected
the soft-start is to be delayed until 20 min following the last sighting
One major issue with these requirementsis immediately apparent in
cases where the airgun array is quite large, resulting in the mitigation
zone being mostly, if not entirely, within the array. As a consequence,
an animal that is 500m away from the centre of the array can, in fact,
be only few metres away from the nearest airgun, potentially suffering
irreversible hearing damage.
This highlights the fact that the arbitrary size of the JNCC exclusion
zone gives little consideration to the actual source levels or the sensitiv-
ity of the species involved (Weir and Dolman, 2007). Elsewhere, only
California and Russia (around Sakhalin Island) are known to select an
operation-based, site-speciﬁc safety zone (Compton et al., 2008;
Nowacek et al., 2013; Weir and Dolman, 2007). To be effective,
exclusion zones should be based on scientiﬁc evidence and consider
the species that are likely to occur in the area, as some species are
more sensitive to noise than others (e.g., McCarthy et al., 2011; Miller,
2011; Miller et al., 2012; Moretti et al., 2010; Pirotta et al., 2012;
Popov et al., 2011a; Tyack et al,., 2011). For operational simplicity,
zone size should be appropriate for the most sensitive species. This is
further reinforced by the discovery that longer noise exposures require
longer periods of hearing recovery following a temporal threshold shift
(TTS) (e.g., Popov et al., 2011b).
The next concern is that the JNCC exclusion zone is only in place
prior to the commencement of the survey, which in itself precludes
the use of shut downs (JNCC, 2010). The utility of this relies entirely
on the assumptions that an animal exposed to the approaching source
will experience gradually increasing sound levels, in the same manner
as a soft-start, and that the animal will react appropriately by moving
away. However, sound levels do not gradually rise with increasing
distance from a source and animals may not react logically (see Pre-
survey mitigation sources: Soft-starts). As a consequence, there are no
guarantees that an animal will not come close enough to be exposed
at dangerous levels. Accordingly, many other countries mandate
shutdowns, thus also requiring the maintenance of the safety zone
during operations (e.g., Australia, Brazil, Colombia, Greenland, New
Zealand; DOC, 2013; Kyhn et al., 2011; MaMa CoCo SEA Project., 2015).
Finally, the JNCC does not even actually mandate the pre-survey
scans. Instead, operations should “whenever possible”begin producing
noise during hours of daylight, so that a pre-activity visual survey can be
completed with the greatest level of conﬁdence (JNCC, 2010).
3.2. Safety zones: Marine Mammal Observers (MMOs)
Marine mammal observers (MMOs) are trained individuals whose
main role under JNCC guidelines (2010) is to search for marine
mammals within a mitigation zone before seismic activity starts. The
role of an MMO is “purely advisory,”as they can only recommend a
2A.J. Wright, A.M. Cosentino / Marine Pollution Bulletin xxx (2015) xxx–xxx
Please cite this article as: Wright, A.J., Cosentino, A.M., JNCC guidelines for minimising the risk of injury and disturbance to marine mammals from
seismic surveys: We can do better, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.08.045
delay in the commencement of the seismic activity if marine mammals
are detected (JNCC, 2010). Additionally, MMOs “advise the crew on the
procedures set out in the JNCC guidelines and provide advice to ensure
that the survey programme is undertaken in accordance with the guide-
lines”as crew members are not obliged to have knowledge of the guide-
lines, and it is not required that a copy be available onboard (JNCC,
2010). Consequently, compliance with the guidelines has its foundation
in the presentation and the MMOs' judgement calls (e.g., distance to a
sighted cetacean) during the survey. This effectively makes them re-
sponsible for compliance as well as monitoring, but without the
power to enforce the provisions of the guidelines in real time.
One of the main problems for MMOs with regard to monitoring a
safety zone is determining the distance between the animal(s) and
the centre of the airgun array. JNCC guidelines recommend the use of
a“range ﬁnding stick”and an equation to estimate where 500 m is
(JNCC, 2010). The most obvious issue with this method is that the
MMO is not placed in the centre of the array. Also, the MMO must
discard the binoculars they use to search for marine mammals before
ﬁnding theanimal(s) again with the naked eye to use the stick. The con-
sequences of this ﬂawed system are not trivial. Detecting a marine
mammal at sea is in itself a difﬁcult task (see below) and this method
introduces unnecessary errors and associated non-compliance. Using
graduated binoculars would improve the situation, although MMOs
are still not situated in the centre of the array. Thus, the mitigation
zone boundary is subjective and imprecise.
Further issues arise when the required distances are beyond the
visual range of the observers, when weather, darkness or sea states
compromise their ability to spot marine mammals (e.g., Barlow and
Gisner, 2006; Harwood and Joynt, 2009; Parente and de Araújo, 2011;
Teilmann, 2003), or when observers have been on duty for too long,
reducing their effectiveness (e.g., Gill et al., 2012; Harwood and Joynt,
2009). Additionally, as MMOs are required to provide their own equip-
ment, magniﬁcation and binocular quality will vary, as will detection
distances and rates.
The level of experience for observers is critical to their ability to de-
tect marine mammals (e.g., Barlow et al., 2006). Even with experienced,
fresh observers and perfect conditions visual surveys are imperfect as
marine mammals spend most of their time underwaterand it is thus en-
tirely possible to miss an animal that is on the survey line (e.g., Thomsen
et al., 2005). Despite this, JNCC-approved MMO training course only
lasts between one and three days, and attendees are not required to
have even seen a marine mammal previously. Training to identify and
monitor marine mammals consists of visual aids (e.g., slide presenta-
tions and drawings: Pers. Obs.) and a ﬁeld trip is not always included.
In some deference to this, these inexperienced MMOs are not allowed
to work in hotspot areas in the UK, however, they can be hired to
work where marine mammals are less abundant, to become ‘experi-
enced’MMOs (JNCC, 2010).
The U.S. Navy are conducting Lookout Effectiveness (LOE) studies, to
compare the relative merits of trained and experienced MMOs against
Navy personnel that have gone through the Navy training program
(see Alexander, 2009). Raw data from one region (Watwood et al.,
2012) suggest that the Navy personnel are not nearly as effective as
more experienced MMOs. Elsewhere the U.S. Navy themselves note
that, “Results are preliminary, but indicate that the U.S. Navy LOs are
not completely effective, and that additional data are needed for more
in-depth evaluation”(U.S. Department of the Navy, DoN, 2013).
In short, it is likely that many marine mammals (especially those
species with low-proﬁle surfacings and small or absent blows) may
stray unseen into the safety zone. This has implications for the level of
protection offered by the JNCC pre-operation safety zone, although it
becomes a much bigger issue for safety zones maintained throughout
operation. Finally, it must be acknowledged that reaching high levels
of compliance does not necessarily mean achieving conservation goals.
Undetected animals and those judged to be further away from the
source than they actually are will suffer the various consequences of
exposure to high/dangerous noise levels in much the same way as if
the guidelines had not been implemented at all (i.e., the same effects
3.3. Safety zones: Passive Acoustic Monitoring (PAM)
The JNCC guidelines have always encouraged the use of PAM to sup-
plement visual surveys in maintaining the safety zone (JNCC, 1998,
2010). Incoming sounds are typically assessed by human operators with
the assistance of one of several software products, but automated detec-
tion is becoming increasingly viable, at least for certain, regularly acoustic
species (e.g., Erbe, 2013). While PAM does solve the issue of detecting
marine mammals that are underwater, it also suffers from a number of
drawbacks (see Bingham, 2011; Gill et al., 2012). Obviously, the system
only works when marine mammals are vocalising and, even then, only
if they are close enough to the hydrophones and using known vocalisation
types. Furthermore, it is not possible to set up software to display the
sounds of all species at once in real time: optimal settings for one species
may reduce the chance of detecting other animals using different frequen-
cies. As with visual observers, operator experience and exhaustion also
come into play (e.g., Barlow and Gisiner, 2006). In contrast, automated
detections are susceptible to variations in the sounds produced by marine
mammals between one population and another, as well as noise, scatter-
ing, spreading and other factors that alter the received sounds.
Distance estimations are needed to determine if an animal is within
the safety zone. The orientation of the sound-producing animal in
relation to the PAM system inﬂuences the levels received and thus
also the estimation of distance to the animal. Using multiple hydro-
phones can address this problem to some extent; however, marine
mammals produce sounds at variable levels.
Consequently, PAM suffers from many of the same issues as visual
surveys (e.g., undetected animals, errors in distance estimations, reli-
ance upon experienced, fresh operators), as well as additional problems
of its own (Bingham, 2011; Gill et al., 2012). However, the technology is
still relatively young and rapidly developing in terms of efﬁciency as a
3.4. Pre-survey mitigation sources: Soft-starts
Soft-starts (also known as ‘ramp-ups’) involve slowly building
source levels of the airguns to operational levels before the survey,
over a period of 20 minutes, “to give adequate time for marine
mammals to leave the area”before being exposed to dangerously high
levels (JNCC, 2010). Once up and running, sound levels will essentially
be continually ramping-up as animals approach the source, or vice
versa. Soft-starts are a long-standing cornerstone of operational guide-
lines for seismic surveys and are increasingly common practice in
sonar exercises and pile driving. However, we are only just beginning
to look into their effectiveness.
Crucially, there are several fundamental assumptions that remain
untested. For example, the procedure relies on the idea that animals
will move away from the source in a logical manner; however, ‘illogical’
responses have been observed. Nowacek et al. (2004) found that right
whales responded to some novel sounds by moving near the surface,
placing them at greatest risk of being stuck by ships. Likewise, manatees
(Trichechus manatus) have been observed responding to boat noise ex-
posure by moving into deep waters, which were typically boat channels
and thus increasing their risks of both higher exposures and being
struck (Miksis-Olds et al., 2007). The ‘logical reaction’assumption also
relies on the further supposition that animals can, and are willing to,
move away from the disturbance. Again, neither may be true. For exam-
ple, coastal and ice-edge areas may ‘trap’animals too close to a source,
or force them into geographical features (e.g., coastlines or sea ice)
that they may be unable to subsequently escape from, with potentially
fatal consequences (e.g., Heide-Jørgensen et al., 2013; Southall et al.,
2013). Similarly, animals may remain in important areas, such as with
3A.J. Wright, A.M. Cosentino / Marine Pollution Bulletin xxx (2015) xxx–xxx
Please cite this article as: Wright, A.J., Cosentino, A.M., JNCC guidelines for minimising the risk of injury and disturbance to marine mammals from
seismic surveys: We can do better, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.08.045
a rich food source, until exposure levels become ‘dangerous’. Alterna-
tively, animals that do leave may be excluded from rich foraging, also
to their detriment.
There are other problems with soft-starts, especially with regard to
moving sources, including: the introduction of additional noise into
the environment; the complications raised by ‘shadow zones’where
levels of noise may be greatly reduced at certain points closer to a source
than wouldbe expected (either as a consequence of propagation related
mostly to oceanographic features or the topography of the area, espe-
cially around coastlines and islands); and the need to carefully consider
the relative speeds of moving sources and marine mammals likely to be
exposed. All of the above have been discussed in greater detail else-
where (e.g., Parsons et al., 2009; Weir and Dolman, 2007); however,
the JNCC (2010) guidelines appear to only be concerned over the addi-
tional noise soft-starts introduce, accordingly setting upper limits on
their maximum duration.
Field studies into the effectiveness of soft-starts are only now being
conducted with seismic surveys and humpback whales in Australia
(e.g., Cato et al., 2012, 2013; Noad et al., 2013). Unfortunately, the avail-
able results are still too few and preliminary to draw any ﬁrm conclusions.
Some assessments have also been made using computer simulations
(e.g., Hannay et al., 2010; von Benda-Beckmann et al., 2014). However
these are, by their very nature, simpliﬁcations that are also based on a
number of unsupported suppositions relating to sound propagation (see
Madsen et al., 2006) and, more importantly, the reactions of the animals
(for a discussion of the importance of this, see Wensveen, 2012).
Soft-starts focus primarily on injury, despite the many other potential
impacts of noise on marine mammals. Thus, it seems inappropriate that a
model result where “no instances were found in which the threshold
levels for hearing injury for cetaceans were reached during the initial
stages of the soft-start sequence”could be used to conclude that,
“animals are not at signiﬁcantly greater risk of harm when a soft-start
is initiated in low visibility conditions”(International Association of Oil
and Gas producers, OGP, 2011). In fact, those responsible for the model-
ling contained within the OGP report (2011) noted that animals would
have time to move away from the source only provided those early expo-
sures were “sensed as disagreeable”(Hannay et al., 2010). Again, these
models do not address the suppositions mentioned above regarding
sound propagation and the behavioural responses of the animals.
While it seems likely that soft starts will reduce the total number of
high-sound level marine mammal exposures to some degree, their
effectiveness remains entirely unknown. The technique is probably
ineffective at eliminating all high-level exposures and may exacerbate
other impacts, such as habitat exclusion (e.g., Culik et al., 2001; Franse,
2005; Gönener and Bilgin, 2009; Haelters and Camphuysen, 2009).
Furthermore, logic holds that if soft-starts were completely effective,
there would never be cause to implement a shutdown, as required in
other parts of the world. In any case, soft-starts must induce potentially
problematic avoidance responses to reduce ‘injury’from dangerously
3.5. Other Mitigation Sources
Mitigation sources are based on the same logic as soft-starts and
thus suffer from many of the same limitations. For example, the JNCC
allows airgun shooting to continue during short breaks in operations
to avoid a full soft-start (e.g., JNCC, 2010). Many mitigation sources
are lower-level sounds (e.g., Kyhn et al., 2011), however the JNCC only
requires that the duty cycle be reduced under certain conditions (as
seems also to be the case for soft-starts, e.g., Figure 3.3., Stone 2015b),
which may actually provide animals enough time to approach close
enough to receive hearing-dangerous exposures, even if all the underly-
ing suppositions are shown to be correct (von Benda-Beckmann et al.,
2014). However, there is little or no scientiﬁc information to assess
effectiveness and it must be acknowledged that mitigation sources
also introduce additional noise.
4. Beyond Injury
4.1. Behavioural responses
As mentioned above, much mitigation of impacts from seismic
surveys (under the JNCC guidelines and elsewhere) seeks to avoid ‘inju-
ry’by inciting behavioural responses, particularly avoidance. However,
there is evidence that behavioural responses to low noise levels may
have greater effects than expected. For example, some strandings of
beaked whales found dead or dying are likely to have resulted from
behavioural reactions to sonar exposures at relatively low noise levels
(e.g., Cox et al., 2006; Hildebrand, 2005; Rommel et al., 2006; Tyack
et al., 2006). In another example, over 1,000 narwhals died in Canada
and Northwest Greenland due to ice entrapments that may have been
the result of seismic survey noise disrupting their normal migration
(Heide-Jørgensen et al., 2013). Other behavioural responses, such as
cessation of singing and the alteration of dive and respiration patterns
(e.g., Gordon et al., 2004) are also likely to occur. The ultimate conse-
quences of these are unknown, but may (at least in some cases) lead
to energetic burdens on the animals (e.g., Williams et al., 2006).
It is thus clear that notable impacts at sub-injurious exposure levels
can arise from behavioural responses. However, such responses are
highly context-dependent. For example, the speciﬁcresponsemay
depend on the activity of the animal at the time of exposure, or any
prior experience that the animal may have (e.g., Andersen et al., 2012;
Robertson et al., 2013). They may also vary depending upon the type
(Melcón et al., 2012) or extent of the disturbance (e.g., La Manna
et al., 2013). This adds further doubts on the general effectiveness of
soft-starts and other mitigation measures.
4.2. Beyond behavioural responses
Injury and behavioural harassment criteria “do not determine the
overall level of impact [as] physiological stress and other factors also
need to be considered”(Fitch et al., 2011). One of these more subtle
factors is the potential for seismic surveys to mask sounds of interest
to marine species. Masking may be a huge issue for mysticetes, which
produce low-frequency signals that may once have allowed them to
communicate over vast distances of hundreds, and possibly thousands,
of kilometres (e.g., Clark et al., 2009; Møhl, 1980, 1981). However, the
effects of masking depend upon many variables, including the frequen-
cies of the sound and the noise, as well as the locations of sources and
Masking may also compromise foraging efforts in ways that we do
not yet understand. For example, the emerging understanding of how
odontocetes hear and discriminate between outgoing and incoming
clicks (Li et al., 2011; Linnenschmidt and Beedholm, 2012) has implica-
tions for how sound could interfere with the interpretation of these
signals (Linnenschmidt and Beedholm, 2012). Noise likely also limits
the ability of marine mammals to sense their environment through
sound. Accordingly, when a whale’s‘communication space’is reduced
through masking (Clark et al., 2009; Hatch et al., 2012) there may be se-
rious repercussions for breeding, foraging and navigation. The potential
for impacts arising from masking in terrestrial species has also been
noted with Francis et al. (2011) even suggesting that acoustic masking
by anthropogenic noise may be a strong selective force shaping the
ecology of birds worldwide.
Animals may use various compensatory mechanisms to counteract
masking, including producing louder sounds or shifting frequencies so
their sounds do not clash with the noise (e.g., Holt et al., 2011). Howev-
er, these mechanisms cannot be applied to sounds of interest produced
by other sources (e.g., prey), may be of variable use depending upon call
type, and likely carry costs to the animal (e.g., Holt et al., 2011, 2015).
These costs may be in terms of energy expenditure or in the form of
reproductive strategy trade-offs, as demonstrated for at least one
singing bird species, the great tit (Halfwerk et al., 2011).
4A.J. Wright, A.M. Cosentino / Marine Pollution Bulletin xxx (2015) xxx–xxx
Other non-behavioural responses include increased stress responses
and the potential for chronic stress (see the extensive review by Wright
and Highﬁll, 2007). There are indications, for example, that ship noise
may increase levels of the stress hormone cortisol in North Atlantic
right whales (Rolland et al., 2012). Even in the absence of a consistent
cortisol response, chronic stress hasbeen associated with serious issues
in other species, including a suppression of both the immune system
and reproduction, disruption of learning and other cognitive functions,
and increased mortality rates (see review by Clark and Stansfeld,
2007). It is reasonable to assume that the constant presence of airgun
noise in some areas could lead to similar effects.
Another related issue is that of attention and distraction. Following
theoretical work by Dukas (2004), data have demonstrated that noise
or disturbance can distract animals from the presence of prey or preda-
tors. Such changes of focus have been observed in Caribbean hermit
crabs (Coenobita clypeatus:Chan et al., 2010), three-spined sticklebacks
(Gasterosteus aculeatus:Purser and Radford, 2011), the shore crab
(Carcinus maenas:Wale et al., 2013), and possibly also greater mouse-
eared bats (Myotis myotis:Siemers and Schaub, 2011). With regard to
cetaceans, Dudok van Heel (1966) proposed that distraction could
potentially lead directly to strandings and recent work suggests that
distraction might also raise mortality indirectly, such as by increasing
bycatch risks in harbour porpoises (e.g., Nielsen et al., 2012; Wright
et al., 2013). With speciﬁc regard to seismic surveys, distraction was
one possible mechanism for increased entanglement rates of humpback
whales (Megaptera novaeangliae) in Brazil during a period of intense
exploratory activity (Todd et al., 1996).
All the above-mentioned subtle and cryptic impacts show that re-
ducing the potential for ‘injury’to individual animals is not sufﬁcient
to prevent detrimental effects to a wider population.
5. JNCC data collection, analysis and reports
While the main role of MMOs on board seismic vessels is to conduct
pre-shooting searches, they are also encouraged to collect data at all
times, provided that such effort is not detrimental to their ability “dur-
ing the crucial time”of pre-survey scanning (JNCC, 2010). As part of
the minimum reporting requirements, at the end of the survey the
MMO report must include speciﬁc information about the size of the
airguns, airgun use and species encountered (JNCC, 2010). With this,
the JNCC has produced summarised reports of the data collected
(Stone, 1997, 1998, 2000, 2003a, 2003b, 2003c; 2006; 2015a,b; Stone
and Tasker, 2006). However, given that MMOs are only required to be
active and thus collect data during pre-survey checks, the scope and
coverage of these reviews are limited accordingly.
Comprehensive management plans should outline a standardised
process for collecting (e.g., methodology), recording and reporting
MMO data, as well as include a more extensive complementary research
program (see Brower et al., 2011). This information can then be fed back
into management decisions, and standard procedures adjusted accord-
ingly. The JNCC guidelines fall short of this ideal in various ways. Firstly,
data collection techniques may vary. Next, there is no speciﬁed process
of feedbackinto the guidelines or any other JNCC process. Perhaps more
importantly, however, is that the level of training and experience
required to become an MMO means that detection and identiﬁcation
of marine mammals isnot guaranteed to beaccurate. Group size estima-
tions and behavioural data (including any changes) may also suffer.
Consequently, it must be accepted that it is not possible to reliably
conclude from this data that any unreported species or behaviours did
These issues are perhaps best highlighted by a sighting of a North
Atlantic right whale (Eubalaena glacialis)reportedbyaMMOinthe
eastern North Atlantic in 2000 (Stone, 2003a). At 200 m distance, the
observer described a great whale lacking a dorsal ﬁn, but did not report
the callosities unique to this species despite recounting a good view of
the head. The North Atlantic right whale is thought to be extirpated in
this area (OSPAR, 2010a). However, if the rest of the MMO’sdescription
is to be believed, it is possible that it details a bowhead whale (Balaena
mysticetus) that strayed beyond its nearby known range (OSPAR,
2010b). Given the highly endangered status of the North Atlantic right
whale (OSPAR, 2010a) the distinction is a very important one. However,
the classiﬁcation of this animal will remain uncertain.
Noise from oil and gas activities is not limited solely to seismic sur-
veys (see Spence et al., 2007). Drilling rigs and drill ships, tankers and
offshore terminals all introduce noise to the environment. However,
none of these have received much focus in terms of noise management
or mitigation, as they are often individually considered to be negligible
sources of noise. This is despite that comprehensive cumulative impact
assessments are required by many countries worldwide. Accordingly, in
consideration of ocean noise, as well as other environmental and
economic factors (e.g., Swift-Hook, 2013), widespread reductions in
the use of (and thus also demand for) oil (and other fossil fuels)
Obviously, this is not going tohappen quickly. Thus interim guidance
is needed. Fortunately, despite initially following the JNCC guidelines,
requirements around the world have generally become more compre-
hensive (Compton et al., 2008). One good example is the guidelines of
the New Zealand Department of Conservation (DOC, 2013). Of particu-
lar note, mitigation zones in New Zealand’s water are dependent upon
array size,the species detected and the presenceof a calf. Upon breaches
of these mitigations zones, MMOs and PAM operators, who must have
on-the-job experience or be supervised by someone that has, are
obliged to call for operational shut-downs (DOC, 2013).
A second good example can be found in Greenland. The guidelines
set out by the Danish Centre for Environment and Energy (DCE: Kyhn
et al., 2011) include not only descriptions of mitigation measures that
should be used (albeit still constrained to an arbitrary 500 m safety
zone), but also requirements for what should be included in Environ-
mental Impact Assessments of planned seismic surveys. For example,
these guidelines require that noise propagation modelling be included,
that these models must take account of all surveys to be carried out in
the area, and that the models are conﬁrmed by acoustic measurements
in the ﬁeld (Kyhn et al., 2011).
The Greenlandic guidelines highlight the fact that operational guide-
lines represent only a small part of the wider management needed for
seismic activities. One alternative approach to addressing this is to set
regulatory limits on the level of sound that can be detected at a given
distance from the source. Based on studies of the sensitivity of harbour
porpoises (Phocoena phocoena) to seismic and pile driving noise
(e.g., Brandt et al., 2013; Lucke et al., 2009; Scheidat et al., 2011), the
German Federal Maritime and Hydrographic Agency requires that pile
driving for offshore wind farms target levels of 160 dB (Sound Exposure
Level –SEL) or 190 dB (peak) at a distance of 750 m (Koschinski and
Lüdemann, 2013). (Note: reference levels were not provided by
Koschinski and Lüdemann, 2013, but we assume the SEL reference
level is 1μPa
-s and the peak reference level is 1μPa.) Initially claimed
to be unachievable,this requirement has driven technological advance-
ments that have since made it possible. Similar restrictions could be
placed on seismic surveys around the world with the same intent.
In fact, certain technical options for reducing noise from seismic
surveys already exist (see Spence et al., 2007; Weilgart, 2010). Further-
more, reducing the proportion of unnecessary sound energy produced
by airguns relative to the amount of useful sound may allow lower
source levels to be used for obtaining the same results (e.g., Ross et al.,
2005). Thus, such standards will not prevent the oil and gas industry
from proceeding with exploration and extraction, or turning proﬁt.
They will, however, drive th e innovation needed to address the environ-
mental consequences of the current technology by reducing the noise
introduced by their arrays.
5A.J. Wright, A.M. Cosentino / Marine Pollution Bulletin xxx (2015) xxx–xxx
Therefore, it is clear that the most appropriate way to address
underwater noise in the mid-term is through the establishment of
scientiﬁcally-based management objectives and the subsequent
development of mitigation measures that can meet these objectives. Ac-
cordingly, governments and regulators are strongly recommended
to implement technology-forcing, scientiﬁcally-based noise limits
for oil and gas activities, including, but not limited to, exploration,
extraction and decommissioning, that can be phased in over a
period of not more than 10 years.
In the short-term, it seems likely that appropriate safety zones in
combination with shutdowns will greatly reduce (but certainly not elim-
inate) the number of marine mammals exposed to high levels of noise,
despite the known limitations. It thus probably remains better to use
pre-operation surveys and safety zones with shutdowns than to proceed
without. However, several factors must be considered to maximise the
effectiveness of these mitigation tools, such as the heavy dependence
of visual surveys upon visibility and the consistent availability of fresh,
experienced observers. While the two recommendations made above
represent new guidance on seismic survey impacts, recent evidence
supports the conclusion of others on the subject of maximising the ef-
fectiveness of current mitigation techniques (e.g., Nowacek et al.,
2013; Parsons et al., 2009; Weir and Dolman, 2007). Thus, if ‘injury’to
marine mammals (and other species) from seismic survey exposure is
to be avoided to the maximum extent practicable, we reiterate (with re-
ﬁnement) the recommendations that management agencies should
include the following requirements in their mitigation guidelines:
•Consideration should be given in the planning stages to unintended
and indirect effects on non-target organisms, both as a result of the
seismic activity and the mitigation measures.
•Safety zones should be manageable, yet biologically relevant and,
whenever possible, species speciﬁc, with a size dependent upon the
sound level of the seismic source and the sound propagation charac-
teristics of the area.
•Safety zones should be maintained throughout a seismic survey, with
shutdowns implemented if a marine mammal is detected within the
•Pre-shoot watchesshould be of appropriate length for species likely to
be encountered, being longer if deep divers are likely present or re-
•Pre-shoot watches should not be commenced during a period of oper-
•A team of visual observers should be deployed, so that two may be
scanning at any given time, with at least one of those being highly ex-
perienced. They should also be furnished with at least one guide for
identifying local species, in case their expertise was gained elsewhere.
•MMOs should have demonstrable experience in observing and/or
studying marine mammals before attending the JNCC approved
MMO training course, which should focus on the legal aspects of the
•Visual observers should not scan for more than 2 hours at a time, to
avoid a drop in their efﬁciency. This requires particular consideration
at high-latitudes with long hours of daylight.
•A minimum requirement for search equipment should be set
(e.g., graduated binoculars) and the use of range sticks should be
•PAM should be used to supplement visual scans, but should only
replace the visual scans entirely in rare cases where the species in
question are known to produce sound for the vast majority of the
time, such as sperm whales and porpoises.
•PAM operators should be additional, dedicated, well-trained personnel
and not simply off-shift visual observers, and also limited to shifts of
not more than 2 hours to avoid efﬁciency reductions.
•PAM systems should be set up to detect the sounds produced by
species that are expected to be in the area, which may require multiple
displays and operators.
•Surveys should not be commenced during periods of restricted visibil-
ity, such as at night or in adverse weather conditions, and should only
continue into these conditions if conditions for using PAM without
visual observers are met.
Given all the above-mentioned limitations, even well-implemented
safety zones are unlikely to protect all marine mammals from danger-
ous exposures. Accordingly, supplementary or alternative impact
reduction efforts (such as new technologies) may be required. In the
meantime, despite the huge uncertainties regarding their effectiveness,
we recommend the continuation of the use of well-designed soft-starts
as a precautionary measure. Soft-starts likely help reduce the total num-
ber of dangerous exposures; however, research is immediately needed
to determine their effectiveness under real world conditionsat reducing
these high-level exposures to marine mammals, as well as to assess
their optimal duration.
There is alsoa pressing need for assessments of the long-term conse-
quences of exposure to seismic surveys and other oil and gas activity on
marine mammals and the ultimate individual and population-level
consequences of the numerous emerging noise-related issues. This is
due to the plethora of non-injurious impacts that will all, to some
extent, be occurring beyond the boundaries of the safety zone. Carefully
designed, long-term studies will be needed that governments should
fund with due haste. While it is not unreasonable to pass on the
costs of this work to the oil and gas industry, independence should be
maintained between the industry and the researchers to retain public
conﬁdence in the results.
Although no funding was directly provided for the preparation of
this manuscript, much of this text is based upon a report written
under contract by AJWfor WWF International. Accordingly, the authors
wish to thank WWF International for this support. Many thanks to
Mikhail Babenko, Thea Bechshøft, Louise Blight, Aimée Leslie, Chris
Parsons, Courtney Smith, Jakob Tougaard, Leslie Walsh and Tonya
Wimmer forall their helpful comments and input during the production
of the original WWF report, as well as two anonymous reviewers whose
comments helped to improve the manuscript.
Alexander, T., 20 09. Essex watches for marine mamm als during Talisman Saber.
(NAVY.mil. Story Number: NNS090718-08. URL: http://www.navy.mil/submit/
Andersen, S.M., Teilmann, J., Dietz, R., Schmidt, N.M., Miller, L.A., 20 12. Behavioural
responses of harbour seals to human-induced disturbances. Aquat. Conserv. Mar.
Freshwat. Ecosyst. 22, 113–121.
Barlow, J., Gisiner, R., 2006. Mitigating, monitoring and assessing the effects of anthropo-
genic sound on beaked whales. J. Cetac. Res. Manage. 7, 239–249.
Barlow, J., Ferguson, M.C., Perrin, W.F., Ballance, L., Gerrodette, T., Joyce,G., MacLeod, C.D.,
Mullin, K., Palka, D.L., Waring, G., 2006. Abundance and densities of beaked and
bottlenose whales (family Ziphiidae). J. Cetac. Res. Manage. 7, 263–270.
Bingham, G. (Ed.), 2011. Status and applications of acoustic mitigation and monitoring
systems for marine mammals: Workshop proceedings; November 17-19, 2009, Bos-
ton, MassachusettsOCS Study BOEMRE 2011-002, New Orleans, LA. U.S. Dept. of the
Interior, Bureau of Ocean Energy Management, Regulation, and Enforcement, Gulf
of Mexico O CS Region.
Brandt, M.J., Höschle, C., Diederichs, A., Betke, K., Matuschek, R., Witte, S., Nehls, G., 2013.
Far-reaching effects of a seal scarer on harbour porpoises, Phocoena phocoena.Aquat.
Conserv. Mar. Freshwat. Ecosyst. 23, 222–232. http://dx.doi.org/10.1002/aqc.2311.
Brower, H., Clark, C.W., Ferguson, M., Gedamke, J., Southall, B., Suydam, R., 2011. Expert panel
review of monitoring protocols in applications for incidental harassment authorizations
related to oil and gas exploration in the Chukchi and Beaufort Seas, 2011: Statoil and
ION Geophysical. (9th March 2011. Anchorage, Alaska. Available at: http://www.
Cato, D., Dunlop, R., Noad, M., McCauley, R., Salgado Kent, C., Kniest, H., Paton, D., Noad, J.,
Jenner,C., 2012. Studies of the effectiveness of ramp-up as a mitigation methodin im-
pacts of noise on marine mammals. Abstract Only. p23 In: 11th European Conference
on Underwater Acoustics, Edinburgh, Scotland, U.K., 2-6 July 2012.
Cato, D., Noad, M., Dunlop, R., McCauley, R., Gales, N.J., Salgado Kent, C.P., Kniest,H., Paton,
D., Jenner, K.C.S., Noad, J., Maggi, A.L., Parnum, I.M., Duncan, A.J., 2013. Astudyofthe
behavioural response of whales to the noise of seismic air guns: design, methods and
progress. Acoust. Aust. 41 (1), 88–97.
6A.J. Wright, A.M. Cosentino / Marine Pollution Bulletin xxx (2015) xxx–xxx
Chan, A.A.Y.H., Stahlman, W.D., Garlick, D., Fast, C.D., Blumstein, D.T., Blaisdell, A.P., 2010.
Increased amplitud e and duration of acoustic stimuli enhance distraction. Anim.
Behav. 80, 1075–1079.
Clark, C.W., Gagnon, G.C., 2006. Considering the temporal and spatial scales of noise
exposures from seismic surveys on baleen whales. International Whaling Commis-
sion Scientiﬁc Committee document SC/58/E9.
Clark, C., Stansfeld, S., 2007. Non-auditory effects of noise on human health: a review of
recent evidence. Int. J. Comp. Psychol. 20 (2-3), 145–158.
Clark, C.W., Ellison, W.T., Southall, B.L., Hatch, L., Van Parijs, S.M., Frankel, A., Ponirakis, D.,
2009. Acoustic masking in marine ecosystems: intuitions, analysis, and implication.
Mar. Ecol. Prog. Ser. 395, 201–222.
Compton, R., Goodwin,L., Handy, R., Abbott,V., 2008. A critical examination of worldwide
guidelines for minimising the disturbance to marine mammals during seismic
surveys. Mar. Policy 32, 255–262.
Cox, T.M., Ragen, T.J., Read, A.J., Vos, E., Baird, R.W., Balcomb, K., Barlow, J., Caldwell, J.,
Cranford, T., Crum, L., D’Amico, A., D’Spain, G., Fernández, A., Finneran, J., Gentry, R.,
Gerth, W., Gulland, F., Hildebrand, J., Houser, D., Hullar, T., Jepson, P.D., Ketten, D.,
MacLeod, C.D., Miller, P., Moore, S., Moundain, D.C., Palka, D., Ponganis, P., Rommel,
S., Rowles, T., Taylor, B., Tyack, P., Wartzok, R. Gisiner, Mead, J., Benner, L., 2006.
Understanding the impacts of anthropogenic sound on beaked whales. J. Cetac. Res.
Manage. 7 (3), 177–187.
Culik, B.M., Koschinski, S., Tregenza, N., Ellis, G.M., 2001. Reactions of harbor porpoises
Phocoena phocoena and herring Clupea harengus to acoustic alarms. Mar. Ecol. Prog.
Ser. 211, 255–260.
DOC (the New Zealand Department of Conservation), 2013. 2013 Code of Conduct for
Minimising Acoustic Disturbance to Marine Mammals from Seismic Survey
Operations. Department of Conservation, Wellington, New Zealand (Available at:
DoN (U.S. Department of the Navy), 2013. Comprehensive exercise and marine species
monitoring report for the U.S. Navy’s Atlantic Fleet Active Sonar Training (AFAST)
and Virginia Capes, Cherry Point, Jacksonville, and Gulf of Mexico range complexes
2009‐2012. Submitted to National Marine Fisheries Service, Ofﬁce of Protected Re-
sources, Silver Spring, Maryland, January 24, 2013 by the Department of the Navy,
United States Fleet Forces Command, Norfolk, Virginia.
DTI (U.K.Department of Trade and Industry),2002. Strategicenvironmentalassessment of
parts of the Central and Southern North Sea SEA 3. (Available at: http://www.
Dudok van Heel, W.H., 1966. Naviga tion in Cetacea. In: Norris, K.D. (Ed.), Whales,
dolphins and porpoises. University of California Press, Berkeley and Los Angeles,
Dukas, R., 2004. Causes and consequences of limited attention. Brain Behav. Evol. 63,
Erbe, C., 2013. Underwater passive acoustic monitoring & noise impacts on marine fauna
–a workshop report. Acoust. Aust. 41 (1), 113–119.
Fitch, R.,Harrison, J., Lewandowski, J., 2011. Marine mammal andsound workshop July13
and 14, 2010. Report to the National Ocean Council Ocean Science and Technology
Interagency Policy Committee. Washington, D.C (Available at: http://www.nmfs.
Francis, C.D., Ortega, C.P., Cruz, A., 2011. Noise pollution ﬁltersbird communities based on
vocal frequency. PLoS One 6 (11), e27052. http://dx.doi.org/10.1371/journal.pone.
Franse, R., 2005. Effectiveness of acoustic deterrent devices (pingers). Universiteit Leiden,
Centrum voor Milieuwetenschappen, Leiden, the Netherlands.
Gill, A., Weir, C., Barton, C., Shrimpton, J., Barrs, J., Barry, S., Lacey, C., Lyne, P., Mustoe, S.,
McRae, H., Rober tson, F., 2012. M arine mammal obs erver association: position
statements. the key issues that should be addressed when developing mitigation
plans to minimise the effects of anthropogenic sound on species of concern. Version
1. Consultation Document –10th September 20 12. Marine Mammal Observer
Association, London, U.K.
Gönener, S., Bilgin, S., 2009. The effect of pingers on harbour porpoise, Phocoena phocoena
bycatch and ﬁshing effort in the turbot gill net ﬁshery in the Turkish Black Sea Coast.
Turk. J. Fish. Aquat. Sci. 9, 151–157.
Goold, J.C., Coates, R.F.W., 2006. Near source, high frequency air-gun signatures. Interna-
tional Whaling Commission Scientiﬁc Committee document SC/58/E30.
Goold, J.C., Fish, P.J., 1998. Broadband spectra of seismic survey air-gun emissions, with
reference to dolphin auditory thresholds. J. Acoust. Soc. Am. 103, 2177–2184.
Gordon, J., Gillespie, D., Potter, J., Frantzis, A., Simmonds, M.P., Swift, R., Thompson, D.,
2004. A review of the effects of seismic surveys on marine mammals. Mar. Technol.
Soc. J. 37, 16–34. http://dx.doi.org/10.4031/002533203787536998.
Haelters, J., Camphuysen, K., 2009. Th e harbour porpoise in the southern North Se a:
abundance, threats and research- and management proposals. Royal Belgian Institute
of Natural Sciences (RBINS/MUMM) and the Royal Netherlands Institute for Sea
Research (NIOZ); report commissioned by the International Fund for Animal Welfare
Halfwerk, W., Bot , S., van der Buikx, J., Velde, M., Komdeur, J., ten Cate, C., Hans
Slabbekoorn, H., 2011. Low-frequency so ngs lose their potency in noisy urba n
conditions. Proc. Natl. Acad. Sci. 108 (35), 14549–14554.
Hannay, D., Racca, R., MacGillivray, A., 2010. Model based assessment of underwater noise
from an airgun array soft-start operation. 8 October 2010. JASCO Applied Sciences.
Victoria,BC. OGP, 2011. Model based assessment of underwaternoise from an airgun
array soft-start operation. OGP Report No. 451. February, 2011. London, U.K.
Harwood, L.A., Joynt, A., 2009. Factors inﬂuencing the effective ness of Marine Mammal
Observers on seismic vessels, with examples from the Canadian Beaufort Sea. Sci.
Advis. Sec. Res. Doc. 2009/048. Department of Fisheries and Oceans Canada.
Hatch, L.T.,Clark, C.W., Van Parijs, S.M., Frankel, A., Ponirakis, D.W., 2012. Quantifyingloss
of acoustic communication space for right whales in and around a U.S. national ma-
rine sanctuary. Conserv. Biol. 26, 983–994. http://dx.doi.org/10.1111/j.1523-1739.
Heide-Jørgensen, M.P., Guldborg Hansen, R., Westdal, K., Reeves, R.R., Mosbech, A., 2013.
Narwhals and seismic exploration: Is seismic noise increasing the risk of ice entrap-
ments? Biol. Conserv. 158, 50–54.
Hermannsen, L., Tougaard, J., Bee dholm, K., Nabe-Nielsen, J., Madsen, P.T., 2015.
Characteristics and propagation of airgun pulses in shallow water with implications
for effects on small marine mammals. PLoS One 10 (7), e0133436. http://dx.doi.
Hildebrand, J.A., 2005. Impacts of anthropogenic sound. In: Reynolds, J.E., Perrin, W.F.,
Reeves, R.R., Montgomery, S., Ragen, T.J. (Eds.), Marine mammal research: Conserva-
tion beyond crisis. The Johns Hopkins University Press, Baltimore, MD, pp. 101–124.
Holt, M.M., Noren, D.P., Emmons, C.K., 2011. Effects of noise levels and call types on the
source levels of killer whale calls. J. Acoust. Soc. Am. 130 (5), 3100–3106.
Holt, M.M., Noren, D.P., Dunkin, R.C., Williams, T.M., 2015. Vocal performance affects
metabolic rate in dolphins: implications for animalscommunicating in noisy environ-
ments. J. Exp. Biol. http://dx.doi.org/ 10.1242/jeb.122424 (Posted online 7th April
Jasny, M., Reynolds, J., Horowitz, C., Wetzler, A., 2005. Sounding the depths. 2nd edition.
Natural Resources Defense Council, New York, NY (Available at: http://www.nrdc.
JNCC (U.K.Joint Nature Conservation Committee),1998. Guidelines forminimising acous-
tic disturbance to marine mammals from seismic surveys. Joint Nature Conservation
Committee, Peterborough, UK.
JNCC (U.K. Joint Nature Conservation Committee), 2010. JNCC guidelines for minimising
the risk of injury and disturbance to marine mammals from seismic surveys August
2010. Joint Nature Conservation Committee, Aberdeen, UK.
JNCC (U.K. Joint Nature Conservation Committee), Natural England, Countryside Council
for Wales, 2010. The protection of marine European Protected Species from injury
and disturbance: Guidance for the marine area in England and Wales and the UK off-
shore marine area. DRAFT. Joint Nature Conservation Committee, Peterborough, UK.
Kliewer, G., 2013. Seismic survey vessel capabilities go up while count goes down. Offshore
(Posted: 8th March 2013. Available at: http://www.offshore-mag.com/articles/print/
Koschinski, S., Lüdemann, K., 2013. Development of noise mitigationmeasures in offshore
wind farm construction 2013. Federal Agency for Nature Conservation (Bundesamt
für Naturschutz, BfN), Hamburg, Ge rmany (Available at: http://tethys.pnnl.gov/
Kyhn, L.A., Boertmann, D., Tougaard, J., Johansen, K., Mosbech, A., 2011. Guidelines to en-
vironmental impact assessment of seismic activities in Greenlandwaters. 3rd revised
edition. Danish Center for Environment and Energy, Roskilde, Denmark Dec. 2011.
La Manna, G., Manghi, M., Pavan, G., Lo Mascolo, F., Sarà, G., 2013. Behavioural strategy of
common bottlenose dolphins (Tursiops truncatus) in response to different kinds of
boats in the water s of Lampedusa Island (Italy). Aquat. Conserv. Ma r. Freshwat.
Ecosyst. 23, 745–757. http://dx.doi.org/10.1002/aqc.2355.
Li, S., Nachtigall, P.E., Breese, M., 2011. Dolp hin hearing during echolocation: evoked
potential responses in an Atlantic bottlenose dolphin (Tursiops truncatus). J. Exp.
Biol. 214, 2027–2035 .
Linnenschmidt, M., Beedholm, K., 2012. What we see is not what they hear: How
porpoises perce ive their outgoi ng clicks. In: Linnenschmidt, M. (E d.), Harbour
porpoise target detection andecho processing abilities. Institute of Biology, University
of Southern Denmark, Odense, pp . 78–87 (Ph.D. Dissertation).
Lubchenco, J., 2010. Memorandum from NOAA Administrator to N. Sutley, Chair of the
Council on Environmental, Quality (Jan. 19, 2010).
Lucke, K., Siebert, U., Lepper, P. A., Blanchet, M.-A., 2009. Temporary shift in masked
hearing thresholds in a harbourporpoise (Phocoena phocoena) after exposure to seis-
mic airgun stimuli. J. Acoust. Soc. Am. 125, 4060–4070.
Madsen, P.T., Johnson, M., Miller, P.J.O., Aguilar Soto, N., Lynch, J., Tyack, P., 2006. Quanti-
tative measures of airgun pulses recordedon sperm whales (Physeter macrocephalus)
using acoustic tags during controlled exposure experiments. J. Acoust. Soc. Am. 120,
MaMa CoCo SEA Project, 2015. A review of seismic mitigation measures used along the
coast of northern south America, from north brazil Up to Colombia 2015. Reference
Document for the MaMa CoCo SEA Steering Committee (Available at: http://www.
McCarthy, E., Moretti,D., Thomas, L., DiMarzio, N., Morrissey, R., Jarvis, S., Ward, J., Izzi, A.,
Dilley, A., 2011. Changes in spatial and temporal distribution and vocal behavior of
Blainville’s beaked whales (Mesoplodon densirostris) during multiship exercises
with mid-frequency sonar. Mar. Mamm. Sci. 27, E206–E226.
Melcón, M.L., Cummins, A.J., Kerosky, S.M., Roche, L.K., Wiggins, S.M., Hildebrand, J.A.,
2012. Blue whales respond to anthropogenic noise. PLoS One 7 (2), e32681. http://
Miksis-Olds, J.L., Donaghay, P.L., Miller, J.H., Tyack, P.L., Reynolds, J.E., 2007. Simulated
vessel approaches elicit differential responses from manatees. Mar. Mamm. Sci. 23
Miller, P., 2011. Cetaceans and naval sonar: behavioral response as a function of sonar
frequency. Annual report to Ofﬁce of Naval Research FY11, under Award Number:
N00014-08-1-0984 (Available at: http://www.onr.navy.mil/reports/FY11/mbmille1.pdf).
Miller, P.J.O., Kvadsheim, P.H., Lam, F.-P.A., Wensveen, P.J., Antunes, R., Catarina Alves, A.,
Visser, F., Kleivane, L., Tyack, P.L., Doksæter Sivle, L., 2012. The severity of behavioral
changes observed during experimental exposures of killer (Orcinus orca), long-ﬁnned
pilot (Globicephala mela s), and sperm (Physeter macroceph alus) whales to naval
sonar. Aquat. Mamm. 38 (4), 362–401. http://dx.doi.org/10.1578/AM.38.4.2012.
7A.J. Wright, A.M. Cosentino / Marine Pollution Bulletin xxx (2015) xxx–xxx
MMC (U.S. Marine Mammal Commission), 2007. Marine mammals and noise –asound
approach to res earch and management. A Report to Congress from the Marine
Mammal Commission (Bethesda, MD. Available at: http://www.mmc.gov/reports/
Møhl, B., 1980. Marine mammals and noise. Arctic Seas Bull. 2, 1–2.
Møhl, B., 1981. Masking effects ofnoise: their distribution in time and space. In: Peterson,
N.M. (Ed.), The question of sound from icebreaker operations: Proceedings from a
workshop. Arctic Pilot Project, Calgary, Alberta, pp. 259–266.
Moretti, D., Marques, T.A., Thomas, L., DiMarzio, N., Dilley, A., Morrissey, R., McCarthy, E.,
Ward, J., Jarvis, S., 2010. A dive counting density estimation method for Blainville’s
beaked whale (Mesoplodon densirostris) using a bottom-mounted hydrophone ﬁeld
as applied to a Mid-Frequency Active (MFA) sonar operation. Appl. Acoust. 71,
Nielsen, T.P., Wahlberg, M., Heikkilä, S., Jensen, M., Sabinsky, P., Dabelsteen, T., 2012.
Swimming patterns of wild harbour porpoises Phocoena phocoena show detection
and avoidance of gillnets at very long ranges. Mar. Ecol. Prog. Ser. 453, 241–248.
Nieukirk, S.L., Stafford, K.M., Mellinger, D.K., Dziak, R.P., Fox, C.G., 2004. Low-frequency
whale and seismic airgun sounds recorded in the mid-Atlantic Ocean. J. Acoust. Soc.
Am. 115 (4), 1832–1843.
Nieukirk, S.L., Mellinger, D.K., Moore, S.E., Klinck, K., Dziak, R.P., Goslin, J., 2012. Sounds
from airguns and ﬁn wh ales recorded in th e mid-Atlantic Ocean, 1999–2009.
J. Acoust. Soc. Am. 131 (2), 1102–1112.
Noad, M.J., Cato, D.H., Dunlop, R.A., McCauley, R., 2013. An interdisciplinary approach to
measuring behavioural impacts of seismic surveys on humpback whales. Abstract
Only In: 27th Conference of the European Cetacean Society: Interdisciplinary
Approaches in the Study of Marine Mammals, 8th-10th April, Setúbal, Portugal, p. 125.
Nowacek, D.P., Johnson, M.P., Tyack, P.L., 2004. North Atlantic right whales (Eubalaena
glacialis) ignore ships but respond to alerting stimuli. Proc. R. Soc. B Biol. Sci. 271,
Nowacek, D.P., Thorne, L.H., Johnston, D.W., Tyack, P.L., 2007. Responses of cetaceans to
anthropogenic noise. Mammal Rev. 37, 81–115.
Nowacek, D.P., Bröker, K., Donovan, G., Gailey, G., Racca, R., Reeves, R.R., Vedenev, A.I.,
Weller, D.W., Southall, B.L., 2013. Responsible practices for minimizing and monitor-
ing environmental impacts of marine seismic surveys with an emphasis on marine
mammals. Aquat. Mamm. 39 (4), 356–377. http://dx.doi.org/10.1578/AM.39.4.2013.
NRC (U.S. National ResearchCouncil), 1994. Low-frequency sound and marine mammals:
current knowledge and research needs. National Academy Press, Washington, D.C.
NRC (U.S. National Research Council), 2000. Marine mammals and low-frequency sound.
National Academy Press, Washington, D.C.
NRC (U.S. National Research Council), 2003. Ocean noise and marine mammals. National
Academy Press, Washington, D.C.
NRC (U.S. National Research Council), 2005. Marine mammal populations and ocean
noise: Determi ning when noise causes biologically signiﬁcant effects. Nation al
Academy Press, Washington, D.C.
OGP (International Association of Oil and Gas Producers), 2011. Model based assessment
of underwater noise from an airgun array soft-start operation. OGP Report No. 451.
February, 2011 (London, U.K).
OGP (International Association of Oil and GasProducers), IAGC (International Association
of Geophysical Contr actors), 2008. Seismic surveys and marine mammals. IAGC,
Houston, TX, USA and OGP, London, UK (Available from: http://www.ogp.org.uk/
OSPAR Commission, 2010a. Background document for northern right whale Eubalaena
glacialis Available at: http://qsr2010.ospar.org/media/assessments/Species/p00496_
OSPAR Commissi on, 2010b. Background document for bowhead whale Balaena
mysticetus. Available at: http://www.ospar .org/documents%5Cdbase%
Parente, C.L., de Araújo, M.E., 2011. Effectiveness of monitoring marine mammals during
marine seismic surveys off Northeast Brazil. Rev Ges Cost Integr 11 (4), 409–419.
Parsons, E.C.M., Dolman, S.J., Jasny, M., Rose, N.A., Simmonds, M.P., Wright, A.J., 2009. A
Critique of the UK’s JNCC Seismic Sur vey Guidelines for minimising acoustic
disturbance to marine mammals: Best Practise? Mar. Pollut. Bull. 58, 643–651.
Pirotta, E., Milor, R., Quick, N., Moretti, D., Di Marzio, N., Tyack, P., Boyd, I., Hastie, G.,
2012. Vessel noise affects beaked whale behavior: results of a dedicated acoustic
response study. PLoS One 7 (8), e42535. http://dx.doi.org/10.1371/journal.pone.
Popov, V.V., Supin, A.Y., Wang, D., Wang, K., Dong, L., Wang, S., 2011a. Noise-induced
temporary threshold shift and recovery in Yangtze ﬁnless porpoises Neophocaena
phocaenoides asiaorientalis. J. Acoust. Soc. Am. 130, 574–584.
Popov, V.V., Klishin,V.O., Nechaev, D.I.,Pletenko, M.G., Rozhnov, V.V., Supin, A.Y.,Sysueva,
E.V., Tarakanov, M.B., 2011b. Inﬂuence of acoustic noises on the white whale hearing
thresholds. Dokl. Biol. Sci. 440, 332–334.
Purser, J., Radford,A.N., 2011. Acousticnoise induces attention shifts and reducesforaging
performance in three-spined sticklebacks (Gasterosteus aculeatus). PLoS One 6 (2),
Richardson, W.J., Greene Jr., C.R., Malme, C.I., Thomson, D.H., 1995. Marine ma mmals and
noise. Academic Press, New York, NY.
Robertson, F.C., Koski, W.R., Thomas, T.A., Richardson, W.J., Würsig, B., Trites, A.W., 2013.
Seismic operationshave variable effects on dive-cycle behavior of bowheadwhales in
the Beaufort Sea. Endanger. Species Res. 21, 143–160. http://d x.doi.org/10.3354/
Rolland, R.M., Parks, S.E., Hunt, K.E., Castellote, M., Corkeron, P.J., Nowacek, D.P., Wasser,
S.K., Kraus, S.D. , 2012. Evidence that ship noise increases stress in right whal es.
Rommel, S.A., Costidi d, A.M., Fernández, A., Jepson, P.D., Pabst, D.A. , McLellan, W.W.,
Houser, D.S., Cranford, T.W., Van Helden, A.L., Allen, D.M., Barros, N.B., 2006.El ements
of beaked whale anatomy and diving physiology and some hypothetical causes of
sonar-related stranding. J. Cetac. Res. Manage. 7, 189–209.
Ross, W., Lee, P., Heiney, S., Young, J., Drake,E., Tenghamn, R., Stenzel, A., 2005. Mitigating
seismicnoise with an acoustic blanket–the promise and the challenge. Lead.Edge 24
(3), 303–313. http://dx.doi.org/10.1190/1.1895317.
Scheidat, M., Tougaard, J., Brasseur, S., Carstensen, J., van Polanen Petel, T., Teilmann, J.,
Reijnders, P., 2011. Harbour porpoises (Phocoena phocoena) and wind farms: a case
study in the Dutch North Sea. Environ. Res. Lett. 6, 025102. http://dx.doi.org/10.
1088/174 8-9326/6 /2/025102 .
Siemers, B.M., Schaub, A., 2011. Hunting at the highway: trafﬁc noise reduces foraging
efﬁciency in acoustic predators. Proc. R. Soc. B Biol. Sci. 278, 1646–1652 (Published
Online 17th November 2010).
Simmonds, M.P., Dolman, S.J., Jasny, M., Parsons, E.C.M., Weilgart, L., Wright, A.J., Leaper,
R., 2014. Marine noise pollution –increasing recognition but need for more practical
action. J. Ocean Technol. 9, 70–90.
Southall, B.L., Bowles, A.E., Ellison, W.T., Finneran, J.J., Gentry, R.L., Greene Jr., C.R., Kastak,
D., Ketten, D.R., Miller, J.H., Nachtigall, P.E., Richardson, W.J., Thomas, J.A., Tyack, P.L.,
2007. Marine mammal noise exposure criteria: initial scientiﬁc recommendations.
Aquat. Mamm. 33 (4), 411–522.
Southall, B.L., Rowles, T., Gulland, F., Baird, R.W., Jepson, P.D., 2013. Final report of the Inde-
pendent Scientiﬁc Review Panel investigating potential contributing factors to a 2008 mass
stranding of melonheaded whales (Peponocephala electra) in Antsohihy. Madagascar
(Available at: http://iwc.int/cache/downloads/4b0mkc030sg0gogkg8kog4o4w/
Spence, J., Fischer, R., Bahtiarian, M., Boroditsky, L., Jones, N.,Dempsey, R., 2007. Review of
existing and future potential treatments for reducingunderwater sound from oil and
gas industry activities. NCE REPORT 07-001. Noise Control Engineering, Inc., Billerica,
Stafford, K.M., Nieukirk, S.L., Fox, C.G., 1999. An acoustic link between blue whales in the
Eastern Tropical Paciﬁc and the Northeast Paciﬁc. Mar. Mamm. Sci. 15, 1258–1268.
Stone, C.J., 1997. The Effects of SeismicActivities on Marine Mammals in UK Waters 1996.
JNCC Report 228. Joint Nature Conservation Committee, Peterborough.
Stone, C.J., 1998. JNCC Report 278. Joint Nature Conservation Committee, Peterborough.
Stone, C.J., 2000. The effects of seismic activities on marine mammals in UKwaters, 1998.
JNCC Report 301. Joint Nature Conservation Committee, Peterborough.
Stone, C.J., 2003a. The effects of seismic activities on marine mammalsin UK waters, 1999.
JNCC Report 316. Joint Nature Conservation Committee, Peterborough.
Stone, C.J., 2003b. The effects of seismic activities on marinemammals in UK waters 2000.
JNCC Report 322. Joint Nature Conservation Committee, Peterborough.
Stone, C.J., 2003c. The effects of seismic activities on marine mammals in UK waters
1998–2000. JNCC Report 323.
Stone, C.J., 2006. Marine mammal observations during seismic surveys in 2001 and 2002.
JNCC Report 359. Joint Nature Conservation Committee, Peterborough.
Stone, C.J., 2015a. Marine mammal observations during seismic surveys from 1994-2010.
JNCC report, No. 463a. Joint Nature Conservation Committee, Peterborough (Available
Stone, C.J., 2015b. Implementation of and considerations for revisions to the JNCC guide-
lines for seismic surveys. JNCC report, No. 463bJoint Nature Conservation Committee,
Peterborough (Available from: http://jncc.defra.gov.uk/page-6986).
Stone, C.J., Tasker, M.L., 2006. The effects of seismic airguns on cetaceans in UK waters.
J. Cetac. Res. Manage. 8, 255–263.
Swift-Hook, D., 2013. The case for renewables apart from global warming.Renew. Energy
49, 147e1 50. http://dx.doi.org/10.1016/j.renene.2012.01.043.
Teilmann, J., 2003. Inﬂuence of sea states on density estimates of harbour porpoises
(Phocoena phocoena). J. Cetac. Res. Manage. 5 (1), 85–92.
Thomsen, F., Ugarte, F., Evans, P.G.H. (Eds.), 2005. Proceedings of the workshop on
estimation of g(0) in line-transect surveys of cetaceans. Held at the European
Cetacean Society’s 18th Annual Conference, Vildmarkshotellet at Kolmården Djur Park,
Kolmården, Sweden, 28th March 2004. ECS Newsletter 44 (Special Issue), April 2005.
Todd, S., Stevick, P., Lien,J., Marques, F., Ketten,D.R., 1996. Behavioural effects of exposure
to underwater explosions in humpback whales (Megaptera novaean- gliae). Can.
J. Zool. 74, 1661–1672.
Tougaard, J., Wright, A.J., Madsen, P.T., 2014. Cetacean noise criteria revisited in the light
of proposedexposure limits for harbourporpoises. Mar. Pollut. Bull. http://dx.doi.org/
10.1016/j.marpolbul.2014.10.051. ) (Published online: 20th Nov 2014).
Tyack, P.L., Johnson, M., Aguilar de Soto, N., Sturlese, A., Madsen, P.T., 2006. Extreme
diving of beaked whales. J. Exp. Biol. 209, 4238–4253.
Tyack, P.L., Zimmer, W.M.X., Moretti, D., Southall, B.L., Claridge, D.E., Durban, J.W., Clark,
C.W., D’Amico, A., DiMarzio, N., Jarvis, S., McCarthy, E., Morrissey, R., Ward, J., Boyd,
I.L., 2011. Beaked whales respond to simulated and actual navy sonar. PLoS One 6
(3), e17009. http://dx.doi.org/10.1371/journal.pone.0017009.
von Benda-Beckmann, A.M., Wensveen, P.J., Kvadsheim, P.H., Lam, F.P.A., Miller, P.J.O.,
Tyack, P.L., Ainslie, M.A., 2014. Modeling ramp-up effectiveness at mitigating impact
of sonar sounds on marine mam mals. Conse rv. Biol. 28, 119–128.
Wale, M.A.,Simpson, S.D., Radford, A.N., 2013. Size-dependent physiological responses of
shore crabs to single and repeated playback of ship noise. Biol. Lett. 9, 20121194.
Watwood, S., Uyeyama, R., Balla-Holden, A., Jefferson, T., 2012. Cruise report, marine
species monitoring and lookout effectiveness study submarine commanders course.
Range Complex, Hawai’i (February 2012).
Weilgart, L.S., 2007. The impacts of anthropogenic ocean noise on cetaceansand implica-
tions for management . Can. J. Z ool. 85, 1091–1116.
Weilgart, L. (Ed.), 2010. Report of the Workshop on Alternative Technologies to Seismic
Airgun Surveys for Oil and Gas Exploration and their Potential for Reducing Impacts
8A.J. Wright, A.M. Cosentino / Marine Pollution Bulletin xxx (2015) xxx–xxx
onMarineMammals.Monterey,CA,USA,31August-1 Sept. 2009. Okeanos - Foundation
for the Sea, Darmstadt (Available at: http://www.okeanos-stiftung.org/assets/Uploads/
Weir, C.R., Dolma n, S.J., 2007. Comparative review of the regional marine mammal
mitigation guidelines implemented during industrial seismic surveys, and guidance
towards a worldwide standard. J Int Wildl Law Policy 10, 1–27.
Wensveen,P.J., 2012. The effects of sound propagation and avoidance behaviour on naval
sonar levels received by cetaceans. Thesis Submitted for the Degree of MPhil at the
University of St. Andrews, Scotland.
Williams, R., Lusseau, D., Hammond, P.S., 2006. Potential energetic cost to killer whales of
disturbance by vessels and the role of a marine protected area. Biol. Conserv. 133 (3),
Wright, A.J., Highﬁll, L., 2007. Considerations of the effects of noise on marine mammals
and other animals. Int. J. Comp. Psychol. 20 (2-3), 89–316.
Wright, A.J., Maar, M., Mohn, C., Nabe-Nielsen, J., Siebert, U., Fast Jensen, L., Baagøe, H.J.,
Teilmann, J., 2013. Possible causes of a harbour porpoise mass stranding in Danish
waters in 2005. PLoS One 8 (2), e55553. http:/ /dx.doi.org/10 .1371/journal.pone.
9A.J. Wright, A.M. Cosentino / Marine Pollution Bulletin xxx (2015) xxx–xxx