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Impacts of Navy Sonar on Whales and Dolphins: Now beyond a Smoking Gun?

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Abstract

The risks military sonar poses to cetaceans received international attention with a highly-publicized mass stranding of Cuvier's beaked whales (Ziphius cavirostris), Blainville's beaked whales (Mesoplodon densirostris), and northern minke whales (Balaenoptera acutorostrata) in the Bahamas in 2000. This was the first time that the US Government determined a stranding to be the result of mid-frequency active sonar use. Subsequently attention has been drawn to other mass strandings coincident with naval exercises, including events preceding the 2000 mass stranding. The list of species for which mass strandings have been linked to naval exercises has also increased to include other beaked whales, dwarf and pygmy sperm whales (Kogia spp.), pilot whales (Globicephala spp.), several dolphin species (Stenella sp. and Delphinus delphis), and harbor porpoises (Phocoena phocoena). In particular, there have been several mass strandings in the northern Indian Ocean coincident with naval exercises—including one of the largest (200–250 dolphins)—which have received little attention. Changes in beaked whale behavior, including evasive maneuvering, have been recorded at received levels below <100 dB re 1 μPa (rms) and mass stranding may occur at received levels potentially as low as 150–170 dB re 1 μPa. There is strong scientific evidence to suggest that a wide range of whale, dolphin and porpoise species can also be impacted by sound produced during military activities, with significant effects occurring at received levels lower than previously predicted. Although there are many stranding events that have occurred coincident with the presence of naval vessels or exercises, it is important to emphasize that even the absence of strandings in a region does not equate to an absence of deaths, i.e., absence of evidence does not mean evidence of absence. Strandings may be undetected, or be unlikely to be observed because of a lack of search effort or due to coastal topography or characteristics. There may also be “hidden” impacts of sonar and exercises not readily observable (e.g., stress responses). Due to the level of uncertainty related to this issue, ongoing baseline monitoring for cetaceans in exercise areas is important and managers should take a precautionary approach to mitigating impacts and protecting species.
REVIEW
published: 13 September 2017
doi: 10.3389/fmars.2017.00295
Frontiers in Marine Science | www.frontiersin.org 1September 2017 | Volume 4 | Article 295
Edited by:
Davide Borelli,
Università di Genova, Italy
Reviewed by:
Elisabeth Slooten,
University of Otago, New Zealand
Aaron N. Rice,
Cornell University, United States
*Correspondence:
E. C. M. Parsons
ecm-parsons@earthlink.net
Specialty section:
This article was submitted to
Ocean Engineering, Technology, and
Solutions for the Blue Economy,
a section of the journal
Frontiers in Marine Science
Received: 27 January 2017
Accepted: 30 August 2017
Published: 13 September 2017
Citation:
Parsons ECM (2017) Impacts of Navy
Sonar on Whales and Dolphins: Now
beyond a Smoking Gun?
Front. Mar. Sci. 4:295.
doi: 10.3389/fmars.2017.00295
Impacts of Navy Sonar on Whales
and Dolphins: Now beyond a
Smoking Gun?
E. C. M. Parsons *
Environmental Science and Policy, George Mason University, Fairfax, VA, United States
The risks military sonar poses to cetaceans received international attention with
a highly-publicized mass stranding of Cuvier’s beaked whales (Ziphius cavirostris),
Blainville’s beaked whales (Mesoplodon densirostris), and northern minke whales
(Balaenoptera acutorostrata) in the Bahamas in 2000. This was the first time that the
US Government determined a stranding to be the result of mid-frequency active sonar
use. Subsequently attention has been drawn to other mass strandings coincident with
naval exercises, including events preceding the 2000 mass stranding. The list of species
for which mass strandings have been linked to naval exercises has also increased to
include other beaked whales, dwarf and pygmy sperm whales (Kogia spp.), pilot whales
(Globicephala spp.), several dolphin species (Stenella sp. and Delphinus delphis), and
harbor porpoises (Phocoena phocoena). In particular, there have been several mass
strandings in the northern Indian Ocean coincident with naval exercises—including one
of the largest (200–250 dolphins)—which have received little attention. Changes in
beaked whale behavior, including evasive maneuvering, have been recorded at received
levels below <100 dB re 1 µPa (rms) and mass stranding may occur at received levels
potentially as low as 150–170 dB re 1 µPa. There is strong scientific evidence to suggest
that a wide range of whale, dolphin and porpoise species can also be impacted by sound
produced during military activities, with significant effects occurring at received levels
lower than previously predicted. Although there are many stranding events that have
occurred coincident with the presence of naval vessels or exercises, it is important to
emphasize that even the absence of strandings in a region does not equate to an absence
of deaths, i.e., absence of evidence does not mean evidence of absence. Strandings
may be undetected, or be unlikely to be observed because of a lack of search effort
or due to coastal topography or characteristics. There may also be “hidden” impacts of
sonar and exercises not readily observable (e.g., stress responses). Due to the level of
uncertainty related to this issue, ongoing baseline monitoring for cetaceans in exercise
areas is important and managers should take a precautionary approach to mitigating
impacts and protecting species.
Keywords: cetacean, beaked whales, mass strandings, sonar, underwater noise, conservation, naval exercises
Parsons Navy Sonar Impacts on Whales and Dolphins
INTRODUCTION
The risks sonar poses to cetaceans received international
attention with a highly-publicized mass stranding of Cuvier’s
beaked whales (Ziphius cavirostris), Blainville’s beaked whales
(Mesoplodon densirostris), and northern minke whales
(Balaenoptera acutorostrata), in the Bahamas, in 2000 (Balcomb
and Claridge, 2001). This was the first time that the US
Government determined a stranding to be the result of mid-
frequency active sonar use1(Anonymous, 2001), although the
link between naval exercises and beaked whale strandings had
first been documented in the 1970s (Van Bree and Kristensen,
1974). Following the Bahamas strandings, concerns started to
be expressed about the threats posed to cetacean populations
by active sonar and scientists started to point to evidence of
more sonar-related strandings in various parts of the world
(Parsons et al., 2008a; Dolman et al., 2011) This concern led
to several court cases in the US and legal injunctions against
military exercises using sonar (Zirbel et al., 2011a); sonar-
related resolutions from international treaty organizations; and
statements of concern by professional organizations (see Parsons
et al., 2008a; Dolman et al., 2011; Simmonds et al., 2014).
Although there was mounting scientific evidence that sonar
could cause impacts on cetaceans, the issue of military sonar
was—as Parsons et al. (2008a) put it—a “smoking gun” in
relation to its possible link to cetacean strandings, injuries
and mortalities. The largely precautionary approach, by legal
bodies and organizations, to protect cetaceans from a possible
and on-going threat, appears to be supported by the general
public. A survey restricted to the Washington DC area found
that 51% of respondents believed that naval sonar impacted
marine mammals and, moreover, three-quarters (75.2%) thought
that the Navy should not be exempt from environmental
regulations during peacetime. They also believed that “sonar
use should be moderated if it impacts cetaceans” (75.8%; p.
49) and there was bipartisan support for such protection
(Zirbel et al., 2011b).
This paper provides an update on the latest scientific data on
the effects of sonar on cetaceans, showing that the impacts of
military sonar on a variety of cetacean species are now more than
a “smoking gun,” that all navies need to fully assess the likely
true extent of these impacts, and immediately implement best
practice, including effective monitoring and mitigation measures.
BEAKED WHALE STRANDINGS
Beaked whale mass strandings are relatively unusual events and
draw attention when they occur (see Parsons et al., 2008a; for a
previous summary).
1Mid-frequency active sonar has a frequency range of 1kHz-10kHz. One of the
systems most frequently used and/or associated with stranding events is the
AN/SQS 53C system (3.5kHz with most energy in the 2.5kHz-4.5Hz range) with
a source level of 235 dB rms re 1 µPa @ 1m. Low frequency active sonar has a
frequency range of 100-500Hz and is utilized at approximately the same source
level as mid-frequency sonar.
An analysis of “atypical” mass strandings2of beaked whales
found enough evidence for a statistically significant correlation
between 12 of these events (out of 126 beaked whale mass
standings since 1950) and naval exercises in the Caribbean and
Mediterranean (D’Amico et al., 2009; Filadelfo et al., 2009a). A
further 27 beaked whale mass stranding events occurred either
adjacent to naval facilities or at the same time as nearby naval
vessels could have been using active sonar (D’Amico et al., 2009;
Filadelfo et al., 2009a). It should be noted that due to a lack of
availability of data on naval sonar use, it is entirely possible more
of these beaked whale mass strandings may have been linked to
naval sonar use, or exercises.
Subsequently, in 2014, five Cuvier’s beaked whales stranded
on the coast of Crete during the Noble Dina 2014 joint exercise
with the Israeli, Greek and US Navies (Dolman, 2014). In early
2015, during the hunt for a Russian submarine off the coast of
western Scotland and Ireland, a further eight Cuvier’s beaked
whales (“atypically”) stranded on the coast of Ireland (Sibylline,
2015). Also in 2015, three beaked whales stranded simultaneously
but in different locations along the southern coast of Guam. It was
confirmed that a joint US-Japanese naval exercise, incorporating
sonar use and anti-submarine activities, was being conducted in
nearby waters when the strandings occurred (23–27 March 2015;
Kuam News, 2015).
There have also been mass strandings where anthropogenic
underwater noise has been suspected to be a factor; however,
there was not enough information to make a link. For example,
in 2008 there was a high level of cetacean strandings reported
(56 animals over a 7-month period)—including Cuvier’s and
Sowerby’s beaked whales (Mesoplodon bidens) and long-finned
pilot whales (Globicephala melas)—off the coast of Ireland and
Scotland (Dolman et al., 2010). However, a full investigation
was not conducted due to the carcasses’ advanced state of
decomposition. In the winter of 2014-15 (Amos, 2015; Siggins,
2015), there was a recurrent increase in Cuvier’s beaked whale
strandings in this region (n=15), which appeared to have
occurred at the same time as a high level of anti-submarine
activity, although active sonar use in this region was denied by
the Royal Navy (Farmer, 2015).
THE RECEIVED LEVELS OF SONAR AND
BEAKED WHALES IMPACTS
In 2007, a US government-convened panel published guidelines
for the level of noise at which injury occurs to cetaceans (Southall
et al., 2007). They considered impulsive sound at levels of 230 dB
re:1 µPa peak pressure was an uppermost “safe” exposure limit
for marine mammals, including beaked whales. The 2007 limit
has since been adopted by many noise producers and managers as
an absolute level at which injury impacts to cetaceans occur [(for
example, a European Union advisory group used these criteria
2These “atypical” mass strandings are when multiple animals come ashore, but
the strandings may occur over sizeable geographic area over a short time frame
(Frantzis, 1998). D’Amico et al. (2009) use a definition of two or more animals
stranding within a six day period over a 40 nautical mile (74km) stretch of
coastline.
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Parsons Navy Sonar Impacts on Whales and Dolphins
for their advice on harmful sound levels in EU waters (Tasker
et al., 2010; Genesis, 2011)]. The approach used by Southall
et al. (2007) has been criticized on methodological and statistical
grounds, such as inconsistency of weighting functions and
problems with pseudo replication that downplay the sensitivity
of animals to sound (Tougaard et al., 2015; Wright, 2015).
For example, the proposed levels were developed using limited
available evidence, where levels at which temporary (TTS) and
permanent threshold shift (PTS) and other responses occur in
a small number of captive cetaceans from a limited number of
species [i.e., common bottlenose dolphins (Tursiops truncatus)
and beluga whales (Delphinapterus leucas)], particularly animals
kept in the US Navy’s marine mammal research facilities. Critics
have noted that trained, captive cetaceans, often in noisy facilities
and exposed to high sound level experiments many times, may
not respond in the same way as naïve, wild animals (Parsons
et al., 2008a; Wright et al., 2009). Scientists studying US captive
cetacean responses to sound have also highlighted that using
these animals to directly predict the behavior of wild animals
can lead to biased and/or inaccurate predictions. Such studies
are “likely not directly transferrable to conspecifics in the wild.
The dolphins have years of experience under stimulus control,
which is a necessary condition for the performance of trained
behaviors, and they live within an environment with significant
boating activity. These factors likely impact the threshold of
responsiveness to sound exposure, potentially in the direction
of habituation or increased tolerance to noise(Houser et al.,
2013, p. 130). In fact, the original panel that published the
230 dB re:1 µPa peak pressure safe level noted that cetacean
strandings, and thus injury and probable death, could occur
at much lower levels due to behavioral changes occurring at
much lower sound levels than their criterion (Southall et al.,
2007). NOAA Fisheries has since introduced updated guidance
(National Marine Fisheries Service, 2016) which, for example,
notes that the 230 dB re:1 µPa peak pressure is an impulsive
(one off) exposure level that could cause PTS in species, such
as beaked whales (224 dB re:1 µPa peak pressure for TTS). The
updated guidance notes that a cumulative sound exposure level
(over 24 h) of 185 dB re 1 µPa2s could likewise cause PTS or
170 dB re 1 µPa2s for TTS (National Marine Fisheries Service,
2016). However, this guidance is written in an extremely technical
format and is far from accessible to non-specialists.
That behavioral impacts occur at lower sources levels than
noted above, is an important caveat is frequently overlooked
by noise managers when developing mitigation measures to
active sonar. Following the 2000 Bahamas mass stranding it was
estimated that these whales were exposed to sound levels no
higher than “160–170 dB re1 µPa @ 1 m for 10–30 s” (p. 286 in
Hildebrand, 2005a); or even 150–160 dB re 1 µPa for 50–150 s
(Hildebrand, 2005b), a level clearly much lower than the (now
widely-used) noise impact guideline level of 230 dB re: 1 µPa
(Southall et al., 2007), which would result in a much larger impact
radius around the active sonar source.
Subsequent at-sea studies investigated the specific responses
of tagged Blainville’s beaked whales to military sonar (n=6).
Tyack et al. (2011) found that one animal stopped feeding above
138 SPL dB (or a cumulative sound exposure level (SEL) of 142
dB re 1 µPa2-s), while a second experiencing a received level of
146 re 1 µPa swam 10s of km away (an average of 54 ±10 km)
from the center of the testing range and remained out of the
area for 2–3 days (McCarthy et al., 2011; Tyack et al., 2011).
The calls of beaked whales in the area also decreased during
sonar exposure and did not recover to pre-exposure levels for
up to 108 h after exposure, although calls were produced even at
estimated exposure levels of 157 dB re 1 µPa (rms) (McCarthy
et al., 2011).
In a more recent study on tagged Cuvier’s beaked whales
(n=2), the animals began to respond at received levels of 89
dB re 1 µPa (rms) by ceasing to beat their tail flukes (DeRuiter
et al., 2013). One animal stopped echolocating, ceased foraging,
and swam rapidly away from the source at a received level of 98
dB re 1 µPa (rms). The avoidance response lasted for 1.6 h. The
other whale demonstrated similar responses, and displayed an
abnormal diving pattern for 7.6 h after exposure to sonar. One
of the whales was incidentally exposed to sonar levels similar
to those that produced a response (78–106 dB re 1 µPa rms)
from a naval vessel that was using sonar 118 km away, according
to the ships’ log (DeRuiter et al., 2013). The researchers stated
that “current US management practices assume that significant
behavioral disruption almost never occurs at exposure levels
this low” (DeRuiter et al., 2013). In fact, significant impacts
to beaked whales could occur at levels lower, and from sound
sources at greater distances from animals, than previously
thought, arguably making current US mitigation guidelines for
mid-frequency active sonar ineffective at preventing wide-scale
impacts to whales.
Miller et al. (2015) determined that Northern bottlenose
whales (Hyperoodon ampullatus) showed a “high sensitivity . . .
to acoustic disturbance, with consequent risk from marine
industrialization and naval activity” (p. 1). At a received
sound pressure level (SPL) of 98 dB re 1 µPa, a tagged whale
turned to approach the sound source, but at a received SPL
of 107 dB re 1 µPa, the whale began moving in an unusually
straight course and then made a near 180turn away from
the source, and performed the longest and deepest dive (94
min, 2339 m) recorded for this species (Miller et al., 2015).
Animal movement parameters differed significantly from
baseline for more than 7 h until the tag fell off 33–36 km
away (Miller et al., 2015). No clicks were emitted during the
response period, indicating cessation of normal echolocation-
based foraging. A sharp decline in both acoustic and visual
detections of conspecifics after exposure suggests other whales
in the area responded similarly (Miller et al., 2015). Sivle et al.
(2015) also noted avoidance behavior by bottlenose whales
to a 1–2 kHz sonar signal, starting at a sound pressure level
of 130 dB re 1 µPa. They noted “severe” responses to the
sonar exposure (as ranked by experts grading the responses),
including cessation of feeding and long-term avoidance
(Sivle et al., 2015).
Reponses to (simulated) sonar signals (3.5–4 kHz) were also
noted for Baird’s beaked whale (Berardius bairdii) by Stimpert
et al. (2014). The researchers noted that “within 3 min of
exposure onset, the tagged whale increased swim speed and body
movement, and continued to show unusual dive behavior for
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Parsons Navy Sonar Impacts on Whales and Dolphins
each of its next three dives,” with reactions by the whale occurring
at a received level of approximately 127 dB re 1 µPa.
A number of studies suggest population-level impacts in
beaked whales from repeated exposures to naval activities
(Dolman and Jasny, 2015). A Blainville’s beaked whale population
on the Navy’s AUTEC naval range, in The Bahamas, had lower
abundance and recruitment success (calf to female ratio) than
another off-range Bahamas population, based on a 15-year
field study (Claridge, 2013). Further, adult females showed high
residency at the navy range, putting them at risk, especially when
pregnant and lactating (Claridge, 2013). In California, naval
activities were proposed as one of two plausible hypotheses, along
with ecosystem change, to explain a precipitous decline in beaked
whale populations in the California Current ecosystem (Moore
and Barlow, 2013).
The studies above document behavioral changes in beaked
whales at relatively low levels of mid-frequency sonar exposure
that can be expected to occur at distances many hundreds of
miles from the sonar source. It should be noted, however, that
the degree of responses by animals, and the received level of
sound at which these responses occur, might be affected by
the context in which the sound is received. For example, a
mother and calf might be more “skittish” than a solitary male; an
animal that urgently needs to feed may show less of a behavioral
change than one that is relatively well-fed; a young animal that
is more vulnerable to predation might react more quickly to
an intense noise than a larger adult; a habituated animal might
respond at higher received levels than a naive animal; or a
chronically stressed animal might responded differently to a non-
stressed animal (see section Absence of Evidence Does Not Mean
Evidence of Absence–the Need For Precaution Below; Beale and
Monaghan, 2004; Beale, 2007; Wright et al., 2007; Guerra et al.,
2014; Forney et al., 2017).
Even if the changes in beaked whale behavior resulting from
sonar use do not lead to stranding events, they could still lead
to sub-lethal impacts and significantly impact the health of
individuals, and potentially populations, by affecting biologically
important behaviors, such as preventing normal feeding or
separating family members. The degree to which this happens
is currently an important question for cetacean conservation, in
all species (e.g., Parsons et al., 2015). For example, even minor
reductions in feeding behavior as the result of human disturbance
were estimated to have dramatic effects on the energy budget
of cetaceans, which could translate into substantive negative
impacts on cetacean fitness and health (Christiansen et al., 2013).
To quantify this energetic impact, Williams et al. (2017) tried
to estimate the energetic cost of beaked whales evading sonar.
Using the energetic costs of bottlenose dolphin fluke strokes
(3.31 ±0.20 J kg1 stroke1), the cost of high speed evasion
responses in cetaceans, including observed escape responses of
beaked whales to naval sonar (increased fluking rates and longer
bursts of powered swimming), was estimated. Williams et al.
(2017) reported a theoretical 30.5% increase in beaked whale
metabolic rate, with an elevated rate being maintained for more
than 90 min after the exposure to noise. Even increasing the
amplitude of vocalizations—so that calls may be heard in a noisy
environment—may have an energetic cost (Holt et al., 2015).
However, the impact of these energetic costs on cetacean health,
both short- and long-term, needs to be evaluated.
There are several modeling efforts underway to estimate the
health and population-level impacts of behavioral disturbances
upon cetacean populations, with beaked whales being a particular
cause for concern. The most notable are the PCOD and PCAD
models (see King et al., 2015 and Harwood et al., 2016 for
details). One particularly enlightening study, on gray whales
(Eschrichtius robustus), predicted that an energy loss of 4%
because of disturbance events during the year of pregnancy
would result in reproductive failure (Villegas-Amtmann, et al.,
2015). Moreover, a 30–35% energy immediately before pregnancy
would mean that a female would lack sufficient energy to become
pregnant (Villegas-Amtmann, et al., 2015). Death would occur
at a 40–42% energy loss (Villegas-Amtmann, et al., 2015). This
equates to a loss of only 10 days of feeding opportunities due to
disturbance theoretically leading to an unsuccessful pregnancy or
loss of a whale calf (Villegas-Amtmann, et al., 2015).
OTHER CETACEAN SPECIES AFFECTED
BY ACTIVE SONAR
A young male beluga whale was exposed to mid-frequency
sound frequencies [19–27 kHz;140–160 dB (no reference level
given)] and exhibited significantly increased heart rate, with
the rate increasing with the intensity of the sound level
(Lyamin et al., 2011). Heart rate increased no matter how
many times the whale was exposed to the sound and the
animal showed no signs of habituation. The respiration rate
of the animal also increased significantly at the beginning of
exposures. Such “severe tachycardia” is the heart’s reaction to
a stressor. This started at very low noise levels (i.e., 140 dB),
suggesting a relatively severe physiological stress response to
anthropogenic noise exposure in this whale. One would expect
similar, substantive, yet not readily observable and effectively
“hidden” stress responses to occur in other cetacean species with
similar physiologies (such as beaked whales). Although short-
term (acute) stress responses are essential for the survival of
animals, allowing them to undergo “fight or flight” responses,
continued (chronic) activation of substantive stress responses can
be physiologically detrimental to animals (Wright et al., 2011).
Tagged blue whales (Balaenoptera musculus) in the Southern
California Bight displayed behavioral responses to experimental
mid-frequency active sonar. Although the sound levels produced
in the experiments were orders of magnitude below most
military systems, the blue whales responded by stopping feeding,
increasing swimming speed and traveling away from the sound
source, with displacement occurring at a received level of
140 dB re 1 µPa, with other responses, such as cessation of
feeding, occurring at lower source levels (Goldbogen et al.,
2013). Baleen whales thus alter biologically important activities
in the presence of sonar sounds. Moreover, the researchers
expressed their concerns that “frequent exposures to mid-
frequency anthropogenic sounds may pose significant risks to the
recovery rates of endangered blue whales” because they ceased
feeding and were displaced (p. 6 in Goldbogen et al., 2013).
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Parsons Navy Sonar Impacts on Whales and Dolphins
Northern minke whales (Balaenoptera acutorostrata) had been
noted previously (Parsons et al., 2008a) to strand during military
sonar-related beaked whale mass stranding events (e.g., in 2000
in the Bahamas and in 2005 in North Carolina; Anonymous,
2001; Balcomb and Claridge, 2001; Hohn et al., 2006). Moreover,
it has been noted that during naval exercises in Scotland, minke
whale sighting rates significantly decreased (Parsons et al., 2000).
It was subsequently proposed that minke whales hear well within
the range of mid-frequency active sonars, and thus they are
likely to be at risk from them over wide ranges, although this
species is often overlooked in exercise planning (Tubelli et al.,
2012). Subsequently, Sivle et al. (2015) found that minke whales
exhibited “high speed avoidance” (p. 469) when exposed to
1–2 kHz sonar signals, with avoidance starting at sound pressure
levels of 130 and 146 dB re 1 µPa,
Minke and blue whales may not be the only baleen whales
that are vulnerable. Between 1982 and 2007, of 180 gray whale
(Eschrichtius robustus) standings that occurred in California,
22% coincided in time and location with military exercises
(Filadelfo et al., 2009b). Although the monthly pattern of whale
strandings in relation to military exercises was statistically
insignificant, nonetheless a substantial proportion of gray whale
strandings did occur coincident with naval exercise periods and
the situation warrants precautionary management and further
investigation into whether this species may also be vulnerable
to military noise (Filadelfo et al., 2009b). Indeed, a study noted
that migrating gray whales moved around a stationary sound
source emitting low frequency active sonar sounds (0.1–0.5 kHz),
based on land-based observations (Buck and Tyack, 2000; Croll
et al., 2001; Tyack, 2009), with avoidance occurring at a received
level of approximately 140 dB re 1 µPa (Buck and Tyack,
2000). Minor movement to avoid a loud sound source may
not seem like a major impact at first glance, but as mentioned
above, Villegas-Amtmann, et al. (2015) estimated that just 10
days of lost foraging opportunities due to disturbance could
lead to an unsuccessful pregnancy/loss of a calf in gray whales
(Villegas-Amtmann, et al., 2015).
Humpback whales (Megaptera novaeangliae) changed their
singing behavior, lengthening their songs—with some ceasing
altogether—when exposed to low frequency active sonar (Miller
et al., 2000). As humpback whale song plays a significant role
in their mating behavior (Parsons et al., 2008b), this may have
biological significance. Sivle et al. (2015) noted humpback whales
responded to 1–2 kHz active sonar, although the responses
were less severe, at received levels higher than did minke and
bottlenose whales. However, Sivle et al. (2016) found that the
first exposure of 12 humpback whales to military low-frequency
sonar (1.3–2.0 kHz with SPLs at the source up to 160–180 dB
re 1 µPa) led to a statistically significant, 68% reduction in
lunge feeding rates. Moreover, during a second exposure, the
feeding rate was 66% below normal, pre-exposure levels. Such
a significant reduction in feeding might have an impact on the
energy budget of these whales.
The following species, other than beaked whales, have
stranded coincident with naval exercises: dwarf sperm whales
(Kogia sima); pygmy sperm whales (K. breviceps); short-finned
pilot whales (Globicephala macrorhynchus); long-finned pilot
whales (G. melas); pygmy killer whales (Feresa attenuata); and
several dolphin species (Stenella attenuata and S. coeruleoalba)
(Kaufman, 2004, 2005; Department of the Environment and
Heritage, 2005; Hohn et al., 2006; Wang and Yang, 2006;
Parsons et al., 2008a). Some of these standings occurred even
though naval vessels were 90 nautical miles away from the
stranding area (Kaufman, 2005)—a distance which is now
known to be within the range that sonar exercises could
potentially cause cetacean behavioral changes (DeRuiter et al.,
2013). It should be noted that the strandings of long-finned
pilot whales were usually associated with high frequency sonar
(50–200 kHz) usage, as opposed to mid-frequency active sonar
(the latter is often considered to be the sound source of most
concern) (Department of the Environment and Heritage, 2005).
Another species that could be added (although not stranding
as such), is the melon-headed whale (Peponocephala electra).
This species has entered unusually shallow waters in response
to sonar exposure—a so-called “milling event” (Southall et al.,
2006).
Even sperm whales (Physeter microcephalus) have been
documented responding to sonar. Isojunno et al. (2016) and
Curé et al. (2016) reported avoidance behavior, interruption of
foraging and/or resting behavior, and an increase in social sound
production in response to 1–2 kHz active sonar. Sperm whales
stopped foraging at cumulative received sound exposure levels
(SEL) of 135–145 dB re 1 µPa (Curé et al., 2016). They also
displayed avoidance and social call changes in response to 6–7
kHz sonar, although the responses were less pronounced (Curé
et al., 2016; Isojunno et al., 2016).
In recent years, more dolphin species have been found during
mass stranding events coincident with naval exercises. In June
2008, a mass stranding of common dolphins (Delphinus delphis)
was associated with a naval exercise in Falmouth Bay, UK and
at least 26 of these animals died. The researchers who evaluated
the standing event determined “naval activity to be the most
probable cause of the Falmouth Bay [mass stranding event]”
(Jepson et al., 2013). One of the largest dolphin stranding events
to date, however, occurred 6–7 March 2009 on Gaddani Beach on
the Balochistan coast of Pakistan, 50 km northwest of Karachi,
when a mass stranding of 200–250 pan-tropical spotted dolphins
(Stenella attenuata) occurred on the second day of a multi-
national naval exercise, AMAN 09 (5–14 March 2009, involving
20+warships from the US, UK, France and Australia) (Kiani
et al., 2011). This event was the largest (atypical) mass stranding
recorded of this species by an order of magnitude. It seems highly
likely that this unusual mass mortality was also caused by naval
exercises.
A common dolphin mass stranding (Delphinis capensis;
n=11) occurred on the Iranian coast on 22 January 2011
(Mohsenian et al., 2014). Although this paper’s authors stated that
they had been told that no Iranian naval activity had occurred
prior to the mass stranding (Mohsenian et al., 2014), a large
multi-national naval exercise involving the Indian, French and
US navies in the Arabian Sea had commenced on 11 January
2011 (Anonymous, 2011). These mass strandings of dolphins in
the northern part of the Indian Ocean have received little to no
attention by government agencies in Europe and the US.
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Parsons Navy Sonar Impacts on Whales and Dolphins
Other delphinids may also be vulnerable to active sonar. For
example, killer whales (Orcinus orca) exposed to mid-frequency
active sonar in Norway responded at received levels much lower
than currently addressed by US Navy mitigation measures (Miller
et al., 2014). In fact, Harris et al. (2015) found that killer whales
were more likely to respond to sonar at lower received levels than
sperm whales or long-finned pilot whales.
Recent research has also highlighted the susceptibility of
porpoises to naval activities. In one incident, 85 harbor porpoises
(Phocoena phocoena) stranded along approximately 100 km of
Danish coastline from 7 to 15 April 2005 (Wright et al., 2013).
Bycatch was established as the cause of death for most of the
individuals, and military vessels from various countries were
confirmed in the area from 7 April, en route to the largest naval
exercise in Danish waters to date (Wright et al., 2013). Although
sonar usage could not be confirmed, it is likely that ships were
testing sonar equipment prior to the main exercise. Thus, naval
activity cannot be ruled out as a possible contributing factor
(Wright et al., 2013).
In fact, recent acoustic exposure experiments suggest that
harbor and finless porpoises (Neophocaena phocaenoides) may be
more sensitive to anthropogenic sound than previously thought.
Previous predictions had extrapolated their sensitivity to sound
based on results from common bottlenose dolphins (Tursiops
truncatus), but experimental results show this appears to have
underestimated the sound levels at which impacts (behavioral
and TTS) to harbor porpoises might occur (Tougaard et al.,
2015). For porpoises, Tougaard et al. (2015) found that impacts
strongly depend on the frequency of the sound, with avoidance
reactions occurring just 40–50 dB above the hearing threshold
for a particular frequency, with TTS occurring at about 100 dB
above the hearing threshold.
There is a substantive and growing body of corroborating
evidence to suggest that a wide range of whale, dolphin
and porpoise species can be impacted by sound produced
during military activities. The risk active sonar poses is not
limited to beaked whales only. In fact, there may be more
individuals of non-beaked whale species that have stranded
coincident with military exercises than beaked whales. In
addition, the level of sound at which impacts can occur is
generally lower than previously believed. Thus, there is an
urgent need for nations to require more strategic and wide-
spread active sonar management. A more concerted effort to
monitor for cetacean strandings, including delphinids, and to
plan mitigation measures for all naval exercises—especially in the
Indian Ocean—is warranted.
ABSENCE OF EVIDENCE DOES NOT MEAN
EVIDENCE OF ABSENCE–THE NEED FOR
PRECAUTION
Although there are many stranding events that have occurred
coincident with the presence of naval vessels or exercises, it is
important to emphasize that even when strandings do not occur
coincident with naval exercises, this does not mean there have
been no deaths or other negative impacts.
It is highly likely that injury or mortality at sea caused by noise
will not be observed, as explained previously (Fernández et al.,
2005; Parsons et al., 2008a). In some locations, even if animals
do strand, it is unlikely carcasses will be observed or recovered,
either because they wash away before they are seen or the location
is too remote for them to be observed at all.
To illustrate this: there have been 11 cetacean mass stranding
events in the Hawaiian Islands in a 22-year period, of which
six have coincided with military exercises (Faerber and Baird,
2010). However, despite the occurrence of beaked whales in
these waters, none of these mass strandings have involved beaked
whales. Through 2006, only nine single beaked whale strandings
were recorded on Hawaii’s coasts (Faerber and Baird, 2010).
Due to this paucity of records of beaked whale strandings, the
US Navy has stated that there are no impacts on vulnerable
beaked whales in this location from military activities (Faerber
and Baird, 2010). However, an analysis of topography and
coastal characteristics indicates that a variety of factors—a lack
of beaked whale habitat close to shore, a prevalence of steep cliffs,
lower human densities on the coast—decreases the likelihood of
strandings occurring and/or being detected in Hawaii compared
to elsewhere (e.g., Canary Islands) (Faerber and Baird, 2010).
Faerber and Baird (2010, p. 610) stated that “it is inappropriate
to conclude there has been no impact on beaked whales from
anthropogenic activity in the Hawaiian Islands.” This conclusion
could be extrapolated to any location where coastal features make
strandings unlikely, or unobservable, or locations where there
is a lack of public awareness about the need to report stranded
cetaceans so necropsies can be done, or a lack of search effort
for cetacean carcasses, at sea or beached, during active sonar
exercises. Moreover, most cetaceans sink upon death (Allison
et al., 1991), which means discovery of any cetacean killed during
exercises in deep waters is unlikely. Indeed, most of the world’s
coastlines can be considered regions of low reporting for cetacean
mortalities.
Decomposition is also relevant, as time is a critical factor
to collecting pathology evidence. For example, Morell et al.
(2015) has developed a novel technique that requires carefully
examining the microscopic hair cells inside the ear of the whale
and appears able to pinpoint damage as well as the frequency of
the damage, which is critical for identifying the sound source.
Ears need to be removed within just a few hours of death to be
analyzed.
Other impacts include biologically important behavioral
changes, over scales that far exceed current management
measures, which are difficult to accurately predict or to take
into account. Moreover, absence of behavioral changes, such as
moving from feeding habitat, is not necessarily an indicator of no
impact. For example, in Australia two sites occupied by dolphins
were investigated–an area where dolphin-watching occurred and
an area undisturbed by dolphin-watching 17 km away. At the site
where there was no dolphin-watching, dolphin behavior changed
more significantly than at the site where dolphin-watching (and
therefore noise disturbance) occurred (Bejder et al., 2006). This
would normally lead to the conclusion that boat traffic had little
impact on animals at the site where dolphin-watching occurred,
i.e., they were habituated, but the study also looked at changes in
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Parsons Navy Sonar Impacts on Whales and Dolphins
dolphin abundance at the two sites over 10 years. The researchers
found that in the area where dolphin-watching occurred, there
was a significant decline in dolphin numbers (14%) linked to an
increase in dolphin-watching activity (Bejder et al., 2006). The
researchers concluded that the most sensitive animals moved
away from the area, but this effect would have been hidden
without more detailed examination. As a result of this study,
the Australian government implemented restrictions on dolphin-
watching boats (to one), and thus reduced disturbance in the
area.
Therefore, even if there are cetaceans still visible in an area
while military exercises are being, or have been, conducted,
managers should not conclude that there has been no effect
on cetaceans in the area. The animals being observed could
possibly be less sensitive animals that have remained in an area,
and more sensitive animals (such as pregnant females) may
have been displaced. Even with detailed observations on the
movement of individual animals in the population, one cannot
say categorically there has been not been a significant impact of a
sound-producing activity.
Moreover, a lack of visible behavioral response by an animal
might be an indication that an animal is extremely stressed
already. A stressed, starving or sick animal may not display any
observable response if they do not have the energy or capability
to react behaviorally; for example, if the disturbance location is
the only viable feeding area, the animal may not leave (Beale
and Monaghan, 2004; Beale, 2007; Wright et al., 2007; Forney
et al., 2017). In short, absence of a behavioral response to noise
does not necessarily translate to absence of a significant or life-
threatening impact. Sonar management should account for this
and a “precautionary” approach should be taken, with efforts
undertaken to minimize noise exposure even though there might
not be immediately obvious impacts upon cetacean behavior.
Finally, there are “hidden” responses by animals that
may not be readily visible. As noted above, animals may
undergo a substantial stress response at relatively low levels of
noise exposure, and chronic stress could well lead to major
physiological and health impacts (Wright et al., 2009). The level
and impacts of stress in populations of animals that face chronic
sound exposure (such as those within sonar testing ranges or in
regular military exercise areas) need to be studied urgently. There
are many non-invasive methods of studying stress hormone
levels in cetaceans that are now viable (Hunt et al., 2013) and
this could be done relatively easily on potentially impacted
populations.
UNCERTAINTY IN MARINE SCIENCE
In Australia, over 10 years of data were required to determine that
there was a disturbance impact on a dolphin population (Bejder
et al., 2006). In the Bahamas, it took 15 years to gather enough
data to note a decline in beaked whale abundance on a military
testing range (Claridge, 2013).
A lack of longitudinal data and studies gathering baseline
data before the onset of sound-producing events are common
problems with cetacean research. In addition, there are logistical
difficulties in collecting data and observing the behavior of
animals that may spend significant amounts of time underwater.
This is particularly true for deep-diving beaked whales, where
the likelihood of detecting a whale at the surface in normal
conditions may only be one in a hundred, according to Barlow
and Gisiner (2006). All militaries need to commit to long-term
surveillance monitoring, as well as impact monitoring.
For numerous reasons, collecting data in the marine
environment is logistically much more difficult, and more
expensive, than in the terrestrial environment (Norse and
Crowder, 2005). For example, for 60 years no one noticed the
extinction of a limpet species (Lottia alveus), even though the area
it inhabited was studded with marine laboratories and stations
(Carlton et al., 1991). Perrin’s beaked whale (Mesoplodon perrini;
Dalebout, 2002) was only discovered recently, and confirmed
sightings of a living individual have yet to be made in the wild,
despite the species inhabiting the waters off California, one of the
most surveyed regions in the US and the world, with probably
one of the greatest densities of marine mammal biologists in the
country.
Because of the high degree of variability and uncertainty
in cetacean data, the ability to detect trends is very limited
(Gerrodette, 1987; Taylor and Gerrodette, 1993; Taylor et al.,
2007), even for well-studied species and populations. It can
take a decade or more to detect a decline in the best studied
dolphin populations (Wilson et al., 1999; Thompson et al., 2000).
Scientific uncertainty is a major problem for assessing cetacean
conservation status (Parsons et al., 2015). However, lack of data
and effort for beaked whales, coupled with difficulties in studying
them, makes discerning their conservation status particularly
difficult (Parsons, 2016). The percentage of precipitous declines
that would not be detected was 90% for beaked whales (where a
precipitous decline is a 50% decrease in abundance in 15 years,
at which point a stock could be legally classified as “depleted”
under the U.S. Marine Mammal Protection Act) (Taylor et al.,
2007). Even where declines in marine mammal populations have
been identified, the ultimate cause of declines can sometimes be
difficult to determine due to a wide range of subtle contributing
factors (Merrick et al., 1987; Alverson, 1992; Marmontel et al.,
1996). The difficulty with monitoring the effects of anthropogenic
impacts on cetaceans and the huge level of uncertainty involved
have been noted as key issues that need to be addressed via
scientific research, in order to better conserve, manage and
protect cetaceans (Agardy et al., 2007; Dolman, 2007; Dolman
and Jasny, 2015; Parsons et al., 2015; Parsons, 2016).
The importance of not delaying conservation action
when a concern exists, but scientific data and analysis have
not incontrovertibly established the threat exists, i.e., “the
precautionary principle,” has been enshrined in a number of
international laws (Hey, 1991), including the 1992 Convention
on Biological Diversity (Principle 15 of the so-called “Rio
Summit”). Because of this level of uncertainty and difficulty
in establishing beyond a reasonable doubt trends and threats
in cetacean populations, it has been argued that in order to
effectively conserve and manage populations one must be
precautionary, as otherwise catastrophic declines in cetacean
populations could occur before science catches up with the
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Parsons Navy Sonar Impacts on Whales and Dolphins
problem (Mayer and Simmonds, 1996; Parsons et al., 2010, 2015;
Parsons, 2016). It may be a long time before technology and
methods are easily available to answer the many still unanswered
questions about the exact nature and degree of the impacts of
sound on cetaceans, especially when we know that many of the
mitigation measures in place for protecting cetaceans against
the impacts of sound are untested “best guesses” or, indeed, are
known to be ineffectual (Parsons et al., 2009). Therefore, it is
essential that as precautionary and conservative an approach
to management is taken as possible with respect to the effects
of military sonar on cetaceans. Although there is now a better
idea of the scale and range of species that are affected, and the
means by which strandings might occur and possibly the levels
of sound that are most harmful, there are still many unknowns.
Management of cetaceans needs to be precautionary because
of these large number of unknowns, and at present this is
mostly not the case. As Simmonds et al. (2014) and Erbe et al.
(forthcoming) note, the science about the impacts of underwater
noise on marine mammals is advancing, but management is
lagging behind.
Many militaries have committed to investigate and mitigate
their activities to protect marine mammals. However, there
is an additional need for militaries to commit to conducting
adequate baseline monitoring in areas where exercises routinely
occur, to understand and to plan better to avoid deaths and,
more importantly, to avoid behavioral impacts at appropriate
ranges, and to mitigate accordingly. There is also a need for
governments to develop criteria for assessing—and to commit
to independently and thoroughly investigate—all atypical mass
strandings in future.
AUTHOR CONTRIBUTIONS
The author confirms being the sole contributor of this work and
approved it for publication.
FUNDING
Publication of this article was supported by a George Mason
University Library open access publishing grant.
ACKNOWLEDGMENTS
I wish to thank Naomi Rose, Sarah Dolman and two reviewers
for their helpful editorial comments on drafts and revisions of
this paper.
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03.007
Conflict of Interest Statement: The author declares that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
The reviewer ES declared a past co-authorship with one of the authors ECMP to
the handling Editor, who ensured that the process met the standards of a fair and
objective review.
Copyright © 2017 Parsons. This is an open-access article distributed under the terms
of the Creative Commons Attribution License (CC BY). The use, distribution or
reproduction in other forums is permitted, provided the original author(s) or licensor
are credited and that the original publication in this journal is cited, in accordance
with accepted academic practice. No use, distribution or reproduction is permitted
which does not comply with these terms.
Frontiers in Marine Science | www.frontiersin.org 11 September 2017 | Volume 4 | Article 295
... Of particular concern are activities involving the deployment of explosives and munitions, and the use of tactical, high-powered sonar technology operating in the lower (LFAS, ∼0.1-2 kHz) and midfrequency bands (MFAS, 3-8 kHz) (Sivle et al., 2012;Goldbogen et al., 2013;Falcone et al., 2017). LFAS and MFAS systems were developed in the 1950s for anti-submarine warfare (D'Amico and Pittenger, 2009;Bernaldo de Quirós et al., 2019), and have been implicated in a number of atypical lethal mass strandings largely involving deep-diving toothed whales from the Ziphiidae family Filadelfo et al., 2009;Fernández et al., 2012;Parsons, 2017). ...
... interpretable in probabilistic terms . In BRSs, this is advantageous for making appropriate predictions of responsiveness that can inform mitigation measures for naval training activities (Parsons, 2017;Harris et al., 2018). ...
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... The process of echolocation is extremely sensitive [166,167] and can provide odontocetes with a "3D view" of their surrounding environment world. This is confirmed by the fact that sonar signals employed by military vessels can confuse and distress whales and dolphins, and even lead to mass strandings [168]. ...
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... whales (e.g. Parsons, 2017). Consequently, considerable research has focused on characterizing behavioral responses of cetaceans to both simulated and actual naval sonar sources (e.g. ...
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... Since then, various sources and impacts of underwater noise have been identified, lengthening the list of potentially harmful activities and adversely affected species. Among the recognized causes of underwater noise are seaborne transportation (McKenna et al. 2012;Erbe et al. 2019), sonar (Parsons 2017), offshore renewable energy (Gill 2005), underwater construction, explosions, airguns, echolocation, and acoustic deterrents (Richardson et al. 1995;National Research Council 2003;CBD 2012). Since the sources yield varying consequences and demand specific mitigation and reduction approaches, this chapter narrows in on only one: noise emitted by commercial vessels. ...
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