Potential Effects of Sonar Testing on Marine Mammals
Will take the time to translate tomorrow….
Full FDA application here …
Sign Petition ….
Two obvious things at stake:
1. Civil Liberty, regulatory prevention of citizens to protest
2. The life of the ocean as we know it …
My pattern recognition extrapolation for those with eyes willing to see ….
lessons learned with this research can be used to control human population through EMF
The Navy has requested authorization for the take of marine mammals
that may occur incidental to training and testing activities in the
Study Area. The Navy has analyzed potential impacts to marine mammals
from impulsive and non-impulsive sound sources and vessel strike.
Other potential impacts to marine mammals from training activities
in the Study Area were analyzed in the Navy’s HSTT DEIS/OEIS, in
consultation with NMFS as a cooperating agency, and determined to be
unlikely to result in marine mammal harassment. Therefore, the Navy has
not requested authorization for take of marine mammals that might occur
incidental to other components of their proposed activities. In this
document, NMFS analyzes the potential effects on marine mammals from
exposure to non-impulsive sound sources (sonar and other active
acoustic sources), impulsive sound sources (underwater detonations and
pile driving), and vessel strikes.
For the purpose of MMPA authorizations, NMFS’ effects assessments
serve four primary purposes: (1) To prescribe the permissible methods
of taking (i.e., Level B harassment (behavioral harassment), Level A
harassment (injury), or mortality, including an identification of the
number and types of take that could occur by harassment or mortality)
and to prescribe other means of effecting the least practicable adverse
impact on such species or stock and its habitat (i.e., mitigation); (2)
to determine whether the specified activity would have a negligible
impact on the affected species or stocks of marine mammals (based on
the likelihood that the activity would adversely affect the species or
stock through effects on annual rates of recruitment or survival); (3)
to determine whether the specified activity would have an unmitigable
adverse impact on the availability of the species or stock(s) for
subsistence uses; and (4) to prescribe requirements pertaining to
monitoring and reporting.
More specifically, for activities involving non-impulsive or
impulsive sources, NMFS’ analysis will identify the probability of
lethal responses, physical trauma, sensory impairment (permanent and
temporary threshold shifts and acoustic masking), physiological
responses (particular stress responses), behavioral disturbance (that
rises to the level of harassment), and social responses (effects to
social relationships) that would be classified as a take and whether
such take would have a negligible impact on such species or stocks.
Vessel strikes, which have the potential to result in incidental take
from direct injury and/or mortality, will be discussed in more detail
in the Estimated Take of Marine Mammals section. In this section, we
will focus qualitatively on the different ways that non-impulsive and
impulsive sources may affect marine mammals (some of which NMFS would
not classify as harassment). Then, in the Estimated Take of Marine
Mammals section, we will relate the potential effects to marine mammals
from non-impulsive and impulsive sources to the MMPA definitions of
Level A and Level B Harassment, along with the potential effects from
vessel strikes, and attempt to quantify those effects.
Non-Impulsive Sources
Direct Physiological Effects
Based on the literature, there are two basic ways that non-
impulsive sources might directly result in physical trauma or damage:
Noise-induced loss of hearing sensitivity (more commonly-called
“threshold shift”) and acoustically mediated bubble growth.
Separately, an animal’s behavioral reaction to an acoustic exposure
might lead to physiological effects that might ultimately lead to
injury or death, which is discussed later in the Stranding section.
Threshold Shift (noise-induced loss of hearing)–When animals
exhibit reduced hearing sensitivity (i.e., sounds must be louder for an
animal to detect them) following exposure to an intense sound or sound
for long duration, it is referred to as a noise-induced threshold shift
(TS). An animal can experience temporary threshold shift (TTS) or
permanent threshold shift (PTS). TTS can last from minutes or hours to
days (i.e., there is complete recovery), can occur in specific
frequency ranges (i.e., an animal might only have a temporary loss of
hearing sensitivity between the frequencies of 1 and 10 kHz), and can
be of varying amounts (for example, an animal’s hearing sensitivity
might be reduced initially by only 6 dB or reduced by 30 dB). PTS is
permanent, but some recovery is possible. PTS can also occur in a
specific frequency range and amount as mentioned above for TTS.
The following physiological mechanisms are thought to play a role
in inducing auditory TS: Effects to sensory hair cells in the inner ear
that reduce their sensitivity, modification of the chemical environment
within the sensory cells, residual muscular activity in the middle ear,
displacement of certain inner ear membranes, increased blood flow, and
post-stimulatory reduction in both efferent and sensory neural output
(Southall et al., 2007). The amplitude, duration, frequency, temporal
pattern, and energy distribution of sound exposure all can affect the
amount of associated TS and the frequency range in which it occurs. As
amplitude and duration of sound exposure increase, so, generally, does
the amount of TS, along with the recovery time. For intermittent
sounds, less TS could occur than compared to a continuous exposure with
the same energy (some recovery could occur between intermittent
exposures depending on the duty cycle between sounds) (Kryter et al.,
1966; Ward, 1997). For example, one short but loud (higher SPL) sound
exposure may induce the same impairment as one longer but softer sound, which in
turn may cause more impairment than a series of several intermittent
softer sounds with the same total energy (Ward, 1997). Additionally,
though TTS is temporary, prolonged exposure to sounds strong enough to
elicit TTS, or shorter-term exposure to sound levels well above the TTS
threshold, can cause PTS, at least in terrestrial mammals (Kryter,
1985). Although in the case of mid- and high-frequency active sonar
(MFAS/HFAS), animals are not expected to be exposed to levels high
enough or durations long enough to result in PTS.
PTS is considered auditory injury (Southall et al., 2007).
Irreparable damage to the inner or outer cochlear hair cells may cause
PTS; however, other mechanisms are also involved, such as exceeding the
elastic limits of certain tissues and membranes in the middle and inner
ears and resultant changes in the chemical composition of the inner ear
fluids (Southall et al., 2007).
Although the published body of scientific literature contains
numerous theoretical studies and discussion papers on hearing
impairments that can occur with exposure to a loud sound, only a few
studies provide empirical information on the levels at which noise-
induced loss in hearing sensitivity occurs in nonhuman animals. For
marine mammals, published data are limited to the captive bottlenose
dolphin, beluga, harbor porpoise, and Yangtze finless porpoise
(Finneran et al., 2000, 2002b, 2003, 2005a, 2007, 2010a, 2010b;
Finneran and Schlundt, 2010; Lucke et al., 2009; Mooney et al., 2009a,
2009b; Popov et al., 2011a, 2011b; Kastelein et al., 2012a; Schlundt et
al., 2000; Nachtigall et al., 2003, 2004). For pinnipeds in water, data
are limited to measurements of TTS in harbor seals, an elephant seal,
and California sea lions (Kastak et al., 1999, 2005; Kastelein et al.,
2012b).
Marine mammal hearing plays a critical role in communication with
conspecifics, and interpretation of environmental cues for purposes
such as predator avoidance and prey capture. Depending on the degree
(elevation of threshold in dB), duration (i.e., recovery time), and
frequency range of TTS, and the context in which it is experienced, TTS
can have effects on marine mammals ranging from discountable to serious
(similar to those discussed in auditory masking, below). For example, a
marine mammal may be able to readily compensate for a brief, relatively
small amount of TTS in a non-critical frequency range that occurs
during a time where ambient noise is lower and there are not as many
competing sounds present. Alternatively, a larger amount and longer
duration of TTS sustained during time when communication is critical
for successful mother/calf interactions could have more serious
impacts. Also, depending on the degree and frequency range, the effects
of PTS on an animal could range in severity, although it is considered
generally more serious because it is a permanent condition. Of note,
reduced hearing sensitivity as a simple function of aging has been
observed in marine mammals, as well as humans and other taxa (Southall
et al., 2007), so we can infer that strategies exist for coping with
this condition to some degree, though likely not without cost.
Acoustically Mediated Bubble Growth–One theoretical cause of
injury to marine mammals is rectified diffusion (Crum and Mao, 1996),
the process of increasing the size of a bubble by exposing it to a
sound field. This process could be facilitated if the environment in
which the ensonified bubbles exist is supersaturated with gas.
Repetitive diving by marine mammals can cause the blood and some
tissues to accumulate gas to a greater degree than is supported by the
surrounding environmental pressure (Ridgway and Howard, 1979). The
deeper and longer dives of some marine mammals (for example, beaked
whales) are theoretically predicted to induce greater supersaturation
(Houser et al., 2001b). If rectified diffusion were possible in marine
mammals exposed to high-level sound, conditions of tissue
supersaturation could theoretically speed the rate and increase the
size of bubble growth. Subsequent effects due to tissue trauma and
emboli would presumably mirror those observed in humans suffering from
decompression sickness.
It is unlikely that the short duration of sonar pings or explosion
sounds would be long enough to drive bubble growth to any substantial
size, if such a phenomenon occurs. However, an alternative but related
hypothesis has also been suggested: Stable bubbles could be
destabilized by high-level sound exposures such that bubble growth then
occurs through static diffusion of gas out of the tissues. In such a
scenario the marine mammal would need to be in a gas-supersaturated
state for a long enough period of time for bubbles to become of a
problematic size.
Yet another hypothesis (decompression sickness) has speculated that
rapid ascent to the surface following exposure to a startling sound
might produce tissue gas saturation sufficient for the evolution of
nitrogen bubbles (Jepson et al., 2003; Fernandez et al., 2005). In this
scenario, the rate of ascent would need to be sufficiently rapid to
compromise behavioral or physiological protections against nitrogen
bubble formation. Alternatively, Tyack et al. (2006) studied the deep
diving behavior of beaked whales and concluded that: “Using current
models of breath-hold diving, we infer that their natural diving
behavior is inconsistent with known problems of acute nitrogen
supersaturation and embolism.” Collectively, these hypotheses can be
referred to as “hypotheses of acoustically mediated bubble growth.”
Although theoretical predictions suggest the possibility for
acoustically mediated bubble growth, there is considerable disagreement
among scientists as to its likelihood (Piantadosi and Thalmann, 2004;
Evans and Miller, 2003). Crum and Mao (1996) hypothesized that received
levels would have to exceed 190 dB in order for there to be the
possibility of significant bubble growth due to supersaturation of
gases in the blood (i.e., rectified diffusion). More recent work
conducted by Crum et al. (2005) demonstrated the possibility of
rectified diffusion for short duration signals, but at SELs and tissue
saturation levels that are highly improbable to occur in diving marine
mammals. To date, energy levels (ELs) predicted to cause in vivo bubble
formation within diving cetaceans have not been evaluated (NOAA,
2002b). Although it has been argued that traumas from some recent
beaked whale strandings are consistent with gas emboli and bubble-
induced tissue separations (Jepson et al., 2003), there is no
conclusive evidence of this. However, Jepson et al. (2003, 2005) and
Fernandez et al. (2004, 2005) concluded that in vivo bubble formation,
which may be exacerbated by deep, long-duration, repetitive dives may
explain why beaked whales appear to be particularly vulnerable to sonar
exposures. Further investigation is needed to further assess the
potential validity of these hypotheses. More information regarding
hypotheses that attempt to explain how behavioral responses to non-
impulsive sources can lead to strandings is included in the Stranding
and Mortality section.
Acoustic Masking
Marine mammals use acoustic signals for a variety of purposes,
which differ among species, but include communication between
individuals, navigation, foraging, reproduction, and learning about their environment (Erbe and Farmer 2000, Tyack 2000).
Masking, or auditory interference, generally occurs when sounds in the
environment are louder than and of a similar frequency to, auditory
signals an animal is trying to receive. Masking is a phenomenon that
affects animals that are trying to receive acoustic information about
their environment, including sounds from other members of their
species, predators, prey, and sounds that allow them to orient in their
environment. Masking these acoustic signals can disturb the behavior of
individual animals, groups of animals, or entire populations.
The extent of the masking interference depends on the spectral,
temporal, and spatial relationships between the signals an animal is
trying to receive and the masking noise, in addition to other factors.
In humans, significant masking of tonal signals occurs as a result of
exposure to noise in a narrow band of similar frequencies. As the sound
level increases, though, the detection of frequencies above those of
the masking stimulus decreases also. This principle is expected to
apply to marine mammals as well because of common biomechanical
cochlear properties across taxa.
Richardson et al. (1995b) argued that the maximum radius of
influence of an industrial noise (including broadband low frequency
sound transmission) on a marine mammal is the distance from the source
to the point at which the noise can barely be heard. This range is
determined by either the hearing sensitivity of the animal or the
background noise level present. Industrial masking is most likely to
affect some species’ ability to detect communication calls and natural
sounds (i.e., surf noise, prey noise, etc.; Richardson et al., 1995).
The echolocation calls of toothed whales are subject to masking by
high frequency sound. Human data indicate low-frequency sound can mask
high-frequency sounds (i.e., upward masking). Studies on captive
odontocetes by Au et al. (1974, 1985, 1993) indicate that some species
may use various processes to reduce masking effects (e.g., adjustments
in echolocation call intensity or frequency as a function of background
noise conditions). There is also evidence that the directional hearing
abilities of odontocetes are useful in reducing masking at the high-
frequencies these cetaceans use to echolocate, but not at the low-to-
moderate frequencies they use to communicate (Zaitseva et al.,1980). A
recent study by Nachtigall and Supin (2008) showed that false killer
whales adjust their hearing to compensate for ambient sounds and the
intensity of returning echolocation signals.
As mentioned previously, the functional hearing ranges of
mysticetes, odontocetes, and pinnipeds underwater all encompass the
frequencies of the sonar sources used in the Navy’s MFAS/HFAS training
exercises. Additionally, almost all species’ vocal repertoires span
across the frequencies of these sonar sources used by the Navy. The
closer the characteristics of the masking signal to the signal of
interest, the more likely masking is to occur. For hull-mounted sonar,
which accounts for the largest takes of marine mammals (because of the
source strength and number of hours it’s conducted), the pulse length
and low duty cycle of the MFAS/HFAS signal makes it less likely that
masking would occur as a result.
Impaired Communication
In addition to making it more difficult for animals to perceive
acoustic cues in their environment, anthropogenic sound presents
separate challenges for animals that are vocalizing. When they
vocalize, animals are aware of environmental conditions that affect the
“active space” of their vocalizations, which is the maximum area
within which their vocalizations can be detected before it drops to the
level of ambient noise (Brenowitz, 2004; Brumm et al., 2004; Lohr et
al., 2003). Animals are also aware of environmental conditions that
affect whether listeners can discriminate and recognize their
vocalizations from other sounds, which is more important than simply
detecting that a vocalization is occurring (Brenowitz, 1982; Brumm et
al., 2004; Dooling, 2004, Marten and Marler, 1977; Patricelli et al.,
2006). Most animals that vocalize have evolved with an ability to make
adjustments to their vocalizations to increase the signal-to-noise
ratio, active space, and recognizability/distinguishability of their
vocalizations in the face of temporary changes in background noise
(Brumm et al., 2004; Patricelli et al., 2006). Vocalizing animals can
make adjustments to vocalization characteristics such as the frequency
structure, amplitude, temporal structure, and temporal delivery.
Many animals will combine several of these strategies to compensate
for high levels of background noise. Anthropogenic sounds that reduce
the signal-to-noise ratio of animal vocalizations, increase the masked
auditory thresholds of animals listening for such vocalizations, or
reduce the active space of an animal’s vocalizations impair
communication between animals. Most animals that vocalize have evolved
strategies to compensate for the effects of short-term or temporary
increases in background or ambient noise on their songs or calls.
Although the fitness consequences of these vocal adjustments remain
unknown, like most other trade-offs animals must make, some of these
strategies probably come at a cost (Patricelli et al., 2006). For
example, vocalizing more loudly in noisy environments may have
energetic costs that decrease the net benefits of vocal adjustment and
alter a bird’s energy budget (Brumm, 2004; Wood and Yezerinac, 2006).
Shifting songs and calls to higher frequencies may also impose
energetic costs (Lambrechts, 1996).
Stress Responses
Classic stress responses begin when an animal’s central nervous
system perceives a potential threat to its homeostasis. That perception
triggers stress responses regardless of whether a stimulus actually
threatens the animal; the mere perception of a threat is sufficient to
trigger a stress response (Moberg, 2000; Sapolsky et al., 2005; Seyle,
1950). Once an animal’s central nervous system perceives a threat, it
mounts a biological response or defense that consists of a combination
of the four general biological defense responses: Behavioral responses,
autonomic nervous system responses, neuroendocrine responses, or immune
responses.
In the case of many stressors, an animal’s first and sometimes most
economical (in terms of biotic costs) response is behavioral avoidance
of the potential stressor or avoidance of continued exposure to a
stressor. An animal’s second line of defense to stressors involves the
sympathetic part of the autonomic nervous system and the classical
“fight or flight” response which includes the cardiovascular system,
the gastrointestinal system, the exocrine glands, and the adrenal
medulla to produce changes in heart rate, blood pressure, and
gastrointestinal activity that humans commonly associate with
“stress.” These responses have a relatively short duration and may or
may not have significant long-term effect on an animal’s welfare.
An animal’s third line of defense to stressors involves its
neuroendocrine systems; the system that has received the most study has
been the hypothalmus-pituitary-adrenal system (also known as the HPA
axis in mammals or the hypothalamus-pituitary-interrenal axis in fish
and some reptiles). Unlike stress responses associated with the
autonomic nervous system, virtually all neuro-endocrine functions that are affected by
stress–including immune competence, reproduction, metabolism, and
behavior–are regulated by pituitary hormones. Stress-induced changes
in the secretion of pituitary hormones have been implicated in failed
reproduction (Moberg, 1987; Rivier, 1995), altered metabolism (Elasser
et al., 2000), reduced immune competence (Blecha, 2000), and behavioral
disturbance. Increases in the circulation of glucocorticosteroids
(cortisol, corticosterone, and aldosterone in marine mammals; see
Romano et al., 2004) have been equated with stress for many years.
The primary distinction between stress (which is adaptive and does
not normally place an animal at risk) and distress is the biotic cost
of the response. During a stress response, an animal uses glycogen
stores that can be quickly replenished once the stress is alleviated.
In such circumstances, the cost of the stress response would not pose a
risk to the animal’s welfare. However, when an animal does not have
sufficient energy reserves to satisfy the energetic costs of a stress
response, energy resources must be diverted from other biotic function,
which impairs those functions that experience the diversion. For
example, when mounting a stress response diverts energy away from
growth in young animals, those animals may experience stunted growth.
When mounting a stress response diverts energy from a fetus, an
animal’s reproductive success and its fitness will suffer. In these
cases, the animals will have entered a pre-pathological or pathological
state which is called “distress” (sensu Seyle 1950) or “allostatic
loading” (sensu McEwen and Wingfield, 2003). This pathological state
will last until the animal replenishes its biotic reserves sufficient
to restore normal function. Note that these examples involved a long-
term (days or weeks) stress response exposure to stimuli.
Relationships between these physiological mechanisms, animal
behavior, and the costs of stress responses have also been documented
fairly well through controlled experiments; because this physiology
exists in every vertebrate that has been studied, it is not surprising
that stress responses and their costs have been documented in both
laboratory and free-living animals (for examples see, Holberton et al.,
1996; Hood et al., 1998; Jessop et al., 2003; Krausman et al., 2004;
Lankford et al., 2005; Reneerkens et al., 2002; Thompson and Hamer,
2000). Information has also been collected on the physiological
responses of marine mammals to exposure to anthropogenic sounds (Fair
and Becker, 2000; Romano et al., 2002; Wright et al., 2008). For
example, Rolland et al. (2012) found that noise reduction from reduced
ship traffic in the Bay of Fundy was associated with decreased stress
in North Atlantic right whales. In a conceptual model developed by the
Population Consequences of Acoustic Disturbance (PCAD) working group,
serum hormones were identified as possible indicators of behavioral
effects that are translated into altered rates of reproduction and
mortality. The Office of Naval Research hosted a workshop (Effects of
Stress on Marine Mammals Exposed to Sound) in 2009 that focused on this
very topic (ONR, 2009).
Studies of other marine animals and terrestrial animals would also
lead us to expect some marine mammals to experience physiological
stress responses and, perhaps, physiological responses that would be
classified as “distress” upon exposure to high frequency, mid-
frequency and low-frequency sounds. For example, Jansen (1998) reported
on the relationship between acoustic exposures and physiological
responses that are indicative of stress responses in humans (for
example, elevated respiration and increased heart rates). Jones (1998)
reported on reductions in human performance when faced with acute,
repetitive exposures to acoustic disturbance. Trimper et al. (1998)
reported on the physiological stress responses of osprey to low-level
aircraft noise while Krausman et al. (2004) reported on the auditory
and physiology stress responses of endangered Sonoran pronghorn to
military overflights. Smith et al. (2004a, 2004b), for example,
identified noise-induced physiological transient stress responses in
hearing-specialist fish (i.e., goldfish) that accompanied short- and
long-term hearing losses. Welch and Welch (1970) reported physiological
and behavioral stress responses that accompanied damage to the inner
ears of fish and several mammals.
Hearing is one of the primary senses marine mammals use to gather
information about their environment and to communicate with
conspecifics. Although empirical information on the relationship
between sensory impairment (TTS, PTS, and acoustic masking) on marine
mammals remains limited, it seems reasonable to assume that reducing an
animal’s ability to gather information about its environment and to
communicate with other members of its species would be stressful for
animals that use hearing as their primary sensory mechanism. Therefore,
we assume that acoustic exposures sufficient to trigger onset PTS or
TTS would be accompanied by physiological stress responses because
terrestrial animals exhibit those responses under similar conditions
(NRC, 2003). More importantly, marine mammals might experience stress
responses at received levels lower than those necessary to trigger
onset TTS. Based on empirical studies of the time required to recover
from stress responses (Moberg, 2000), we also assume that stress
responses are likely to persist beyond the time interval required for
animals to recover from TTS and might result in pathological and pre-
pathological states that would be as significant as behavioral
responses to TTS.
Behavioral Disturbance
Behavioral responses to sound are highly variable and context-
specific. Many different variables can influence an animal’s perception
of and response to (nature and magnitude) an acoustic event. An
animal’s prior experience with a sound or sound source effects whether
it is less likely (habituation) or more likely (sensitization) to
respond to certain sounds in the future (animals can also be innately
pre-disposed to respond to certain sounds in certain ways) (Southall et
al., 2007). Related to the sound itself, the perceived nearness of the
sound, bearing of the sound (approaching vs. retreating), similarity of
a sound to biologically relevant sounds in the animal’s environment
(i.e., calls of predators, prey, or conspecifics), and familiarity of
the sound may affect the way an animal responds to the sound (Southall
et al., 2007). Individuals (of different age, gender, reproductive
status, etc.) among most populations will have variable hearing
capabilities, and differing behavioral sensitivities to sounds that
will be affected by prior conditioning, experience, and current
activities of those individuals. Often, specific acoustic features of
the sound and contextual variables (i.e., proximity, duration, or
recurrence of the sound or the current behavior that the marine mammal
is engaged in or its prior experience), as well as entirely separate
factors such as the physical presence of a nearby vessel, may be more
relevant to the animal’s response than the received level alone.
Exposure of marine mammals to sound sources can result in no
response or responses including, but not limited to: increased
alertness; orientation or attraction to a sound source; vocal
modifications; cessation of feeding;
cessation of social interaction; alteration of movement or diving
behavior; habitat abandonment (temporary or permanent); and, in severe
cases, panic, flight, stampede, or stranding, potentially resulting in
death (Southall et al., 2007). A review of marine mammal responses to
anthropogenic sound was first conducted by Richardson and others in
1995. A more recent review (Nowacek et al., 2007) addresses studies
conducted since 1995 and focuses on observations where the received
sound level of the exposed marine mammal(s) was known or could be
estimated. The following sub-sections provide examples of behavioral
responses that provide an idea of the variability in behavioral
responses that would be expected given the differential sensitivities
of marine mammal species to sound and the wide range of potential
acoustic sources to which a marine mammal may be exposed. Estimates of
the types of behavioral responses that could occur for a given sound
exposure should be determined from the literature that is available for
each species, or extrapolated from closely related species when no
information exists.
Flight Response–A flight response is a dramatic change in normal
movement to a directed and rapid movement away from the perceived
location of a sound source. Relatively little information on flight
responses of marine mammals to anthropogenic signals exist, although
observations of flight responses to the presence of predators have
occurred (Connor and Heithaus, 1996). Flight responses have been
speculated as being a component of marine mammal strandings associated
with sonar activities (Evans and England, 2001).
Response to Predator–Evidence suggests that at least some marine
mammals have the ability to acoustically identify potential predators.
For example, harbor seals that reside in the coastal waters off British
Columbia are frequently targeted by certain groups of killer whales,
but not others. The seals discriminate between the calls of threatening
and non-threatening killer whales (Deecke et al., 2002), a capability
that should increase survivorship while reducing the energy required
for attending to and responding to all killer whale calls. The
occurrence of masking or hearing impairment provides a means by which
marine mammals may be prevented from responding to the acoustic cues
produced by their predators. Whether or not this is a possibility
depends on the duration of the masking/hearing impairment and the
likelihood of encountering a predator during the time that predator
cues are impeded.
Diving–Changes in dive behavior can vary widely. They may consist
of increased or decreased dive times and surface intervals as well as
changes in the rates of ascent and descent during a dive. Variations in
dive behavior may reflect interruptions in biologically significant
activities (e.g., foraging) or they may be of little biological
significance. Variations in dive behavior may also expose an animal to
potentially harmful conditions (e.g., increasing the chance of ship-
strike) or may serve as an avoidance response that enhances
survivorship. The impact of a variation in diving resulting from an
acoustic exposure depends on what the animal is doing at the time of
the exposure and the type and magnitude of the response.
Nowacek et al. (2004) reported disruptions of dive behaviors in
foraging North Atlantic right whales when exposed to an alerting
stimulus, an action, they noted, that could lead to an increased
likelihood of ship strike. However, the whales did not respond to
playbacks of either right whale social sounds or vessel noise,
highlighting the importance of the sound characteristics in producing a
behavioral reaction. Conversely, Indo-Pacific humpback dolphins have
been observed to dive for longer periods of time in areas where vessels
were present and/or approaching (Ng and Leung, 2003). In both of these
studies, the influence of the sound exposure cannot be decoupled from
the physical presence of a surface vessel, thus complicating
interpretations of the relative contribution of each stimulus to the
response. Indeed, the presence of surface vessels, their approach, and
speed of approach, seemed to be significant factors in the response of
the Indo-Pacific humpback dolphins (Ng and Leung, 2003). Low frequency
signals of the Acoustic Thermometry of Ocean Climate (ATOC) sound
source were not found to affect dive times of humpback whales in
Hawaiian waters (Frankel and Clark, 2000) or to overtly affect elephant
seal dives (Costa et al., 2003). They did, however, produce subtle
effects that varied in direction and degree among the individual seals,
illustrating the equivocal nature of behavioral effects and consequent
difficulty in defining and predicting them.
Due to past incidents of beaked whale strandings associated with
sonar operations, feedback paths are provided between avoidance and
diving and indirect tissue effects. This feedback accounts for the
hypothesis that variations in diving behavior and/or avoidance
responses can possibly result in nitrogen tissue supersaturation and
nitrogen off-gassing, possibly to the point of deleterious vascular
bubble formation (Jepson et al., 2003). Although hypothetical,
discussions surrounding this potential process are controversial.
Foraging–Disruption of feeding behavior can be difficult to
correlate with anthropogenic sound exposure, so it is usually inferred
by observed displacement from known foraging areas, the appearance of
secondary indicators (e.g., bubble nets or sediment plumes), or changes
in dive behavior. Noise from seismic surveys was not found to impact
the feeding behavior in western grey whales off the coast of Russia
(Yazvenko et al., 2007) and sperm whales engaged in foraging dives did
not abandon dives when exposed to distant signatures of seismic airguns
(Madsen et al., 2006). Balaenopterid whales exposed to moderate low-
frequency signals similar to the ATOC sound source demonstrated no
variation in foraging activity (Croll et al., 2001), whereas five out
of six North Atlantic right whales exposed to an acoustic alarm
interrupted their foraging dives (Nowacek et al., 2004). Although the
received sound pressure levels were similar in the latter two studies,
the frequency, duration, and temporal pattern of signal presentation
were different. These factors, as well as differences in species
sensitivity, are likely contributing factors to the differential
response. A determination of whether foraging disruptions incur fitness
consequences will require information on or estimates of the energetic
requirements of the individuals and the relationship between prey
availability, foraging effort and success, and the life history stage
of the animal.
Breathing–Variations in respiration naturally vary with different
behaviors and variations in respiration rate as a function of acoustic
exposure can be expected to co-occur with other behavioral reactions,
such as a flight response or an alteration in diving. However,
respiration rates in and of themselves may be representative of
annoyance or an acute stress response. Mean exhalation rates of gray
whales at rest and while diving were found to be unaffected by seismic
surveys conducted adjacent to the whale feeding grounds (Gailey et al.,
2007). Studies with captive harbor porpoises showed increased
respiration rates upon introduction of acoustic alarms (Kastelein et
al., 2001; Kastelein et al., 2006a) and emissions for underwater data
transmission (Kastelein et al., 2005). However, exposure of the same
acoustic alarm to a striped dolphin under the same conditions did not
elicit a response (Kastelein et al., 2006a), again highlighting the
importance in understanding species differences in the tolerance of
underwater noise when determining the potential for impacts resulting
from anthropogenic sound exposure.
Social relationships–Social interactions between mammals can be
affected by noise via the disruption of communication signals or by the
displacement of individuals. Disruption of social relationships
therefore depends on the disruption of other behaviors (e.g., caused
avoidance, masking, etc.) and no specific overview is provided here.
However, social disruptions must be considered in context of the
relationships that are affected. Long-term disruptions of mother/calf
pairs or mating displays have the potential to affect the growth and
survival or reproductive effort/success of individuals, respectively.
Vocalizations (also see Masking Section)–Vocal changes in response
to anthropogenic noise can occur across the repertoire of sound
production modes used by marine mammals, such as whistling,
echolocation click production, calling, and singing. Changes may result
in response to a need to compete with an increase in background noise
or may reflect an increased vigilance or startle response. For example,
in the presence of low-frequency active sonar, humpback whales have
been observed to increase the length of their “songs” (Miller et al.,
2000; Fristrup et al., 2003), possibly due to the overlap in
frequencies between the whale song and the low-frequency active sonar.
A similar compensatory effect for the presence of low-frequency vessel
noise has been suggested for right whales; right whales have been
observed to shift the frequency content of their calls upward while
reducing the rate of calling in areas of increased anthropogenic noise
(Parks et al., 2007). Killer whales off the northwestern coast of the
U.S. have been observed to increase the duration of primary calls once
a threshold in observing vessel density (e.g., whale watching) was
reached, which has been suggested as a response to increased masking
noise produced by the vessels (Foote et al., 2004). In contrast, both
sperm and pilot whales potentially ceased sound production during the
Heard Island feasibility test (Bowles et al., 1994), although it cannot
be absolutely determined whether the inability to acoustically detect
the animals was due to the cessation of sound production or the
displacement of animals from the area.
Avoidance–Avoidance is the displacement of an individual from an
area as a result of the presence of a sound. Richardson et al., (1995)
noted that avoidance reactions are the most obvious manifestations of
disturbance in marine mammals. It is qualitatively different from the
flight response, but also differs in the magnitude of the response
(i.e., directed movement, rate of travel, etc.). Oftentimes avoidance
is temporary, and animals return to the area once the noise has ceased.
Longer term displacement is possible, however, which can lead to
changes in abundance or distribution patterns of the species in the
affected region if they do not become acclimated to the presence of the
sound (Blackwell et al., 2004; Bejder et al., 2006; Teilmann et al.,
2006). Acute avoidance responses have been observed in captive
porpoises and pinnipeds exposed to a number of different sound sources
(Kastelein et al., 2001; Finneran et al., 2003; Kastelein et al.,
2006a; Kastelein et al., 2006b). Short-term avoidance of seismic
surveys, low frequency emissions, and acoustic deterrents have also
been noted in wild populations of odontocetes (Bowles et al., 1994;
Goold, 1996; 1998; Stone et al., 2000; Morton and Symonds, 2002) and to
some extent in mysticetes (Gailey et al., 2007), while longer term or
repetitive/chronic displacement for some dolphin groups and for
manatees has been suggested to be due to the presence of chronic vessel
noise (Haviland-Howell et al., 2007; Miksis-Olds et al., 2007).
Maybaum (1993) conducted sound playback experiments to assess the
effects of MFAS on humpback whales in Hawaiian waters. Specifically,
she exposed focal pods to sounds of a 3.3-kHz sonar pulse, a sonar
frequency sweep from 3.1 to 3.6 kHz, and a control (blank) tape while
monitoring behavior, movement, and underwater vocalizations. The two
types of sonar signals (which both contained mid- and low-frequency
components) differed in their effects on the humpback whales, but both
resulted in avoidance behavior. The whales responded to the pulse by
increasing their distance from the sound source and responded to the
frequency sweep by increasing their swimming speeds and track
linearity. In the Caribbean, sperm whales avoided exposure to mid-
frequency submarine sonar pulses, in the range of 1000 Hz to 10,000 Hz
(IWC 2005).
Kvadsheim et al., (2007) conducted a controlled exposure experiment
in which killer whales fitted with D-tags were exposed to mid-frequency
active sonar (Source A: a 1.0 second upsweep 209 dB @ 1-2 kHz every 10
seconds for 10 minutes; Source B: with a 1.0 second upsweep 197 dB @ 6-
7 kHz every 10 seconds for 10 minutes). When exposed to Source A, a
tagged whale and the group it was traveling with did not appear to
avoid the source. When exposed to Source B, the tagged whales along
with other whales that had been carousel feeding, ceased feeding during
the approach of the sonar and moved rapidly away from the source. When
exposed to Source B, Kvadsheim and his co-workers reported that a
tagged killer whale seemed to try to avoid further exposure to the
sound field by the following behaviors: immediately swimming away
(horizontally) from the source of the sound; engaging in a series of
erratic and frequently deep dives that seemed to take it below the
sound field; or swimming away while engaged in a series of erratic and
frequently deep dives. Although the sample sizes in this study are too
small to support statistical analysis, the behavioral responses of the
orcas were consistent with the results of other studies.
In 2007, the first in a series of behavioral response studies, a
collaboration by the Navy, NMFS, and other scientists showed one beaked
whale (Mesoplodon densirostris) responding to an MFAS playback. Tyack
et al. (2011) indicates that the playback began when the tagged beaked
whale was vocalizing at depth (at the deepest part of a typical feeding
dive), following a previous control with no sound exposure. The whale
appeared to stop clicking significantly earlier than usual, when
exposed to mid-frequency signals in the 130-140 dB (rms) received level
range. After a few more minutes of the playback, when the received
level reached a maximum of 140-150 dB, the whale ascended on the slow
side of normal ascent rates with a longer than normal ascent, at which
point the exposure was terminated. The results are from a single
experiment and a greater sample size is needed before robust and
definitive conclusions can be drawn.
Tyack et al. (2011) also indicates that Blainville’s beaked
whales–a resident species within the study area–appear to be
sensitive to noise at levels well below expected TTS (~160 dB
re1[micro]Pa). This sensitivity is manifest by an adaptive movement
away from a sound source. This response was observed irrespective of
whether the signal transmitted was within the band width of MFAS, which
suggests that beaked whales may not respond to the specific sound
signatures. Instead, they may be sensitive to any pulsed sound from a
point source in this frequency range. The response to such stimuli
appears to involve maximizing the distance from the sound source.
Results from a 2007-2008 study conducted near the Bahamas showed a
change in diving behavior of an adult Blainville’s beaked whale to
playback of mid-frequency source and predator sounds (Boyd et al.,
2008; Tyack et al., 2011). Reaction to mid-frequency sounds included
premature cessation of clicking and termination of a foraging dive, and
a slower ascent rate to the surface. Preliminary results from a similar
behavioral response study in southern California waters have been
presented for the 2010-2011 field season (Southall et al., 2011).
Cuvier’s beaked whale responses suggested particular sensitivity to
sound exposure as consistent with results for Blainville’s beaked
whale. Similarly, beaked whales exposed to sonar during British
training exercises stopped foraging (DSTL 2007), and preliminary
results of controlled playback of sonar may indicate feeding/foraging
disruption of killer whales and sperm whales (Miller et al., 2011).
Orientation–A shift in an animal’s resting state or an attentional
change via an orienting response represent behaviors that would be
considered mild disruptions if occurring alone. As previously
mentioned, the responses may co-occur with other behaviors; for
instance, an animal may initially orient toward a sound source, and
then move away from it. Thus, any orienting response should be
considered in context of other reactions that may occur.
There are few empirical studies of avoidance responses of free-
living cetaceans to MFAS. Much more information is available on the
avoidance responses of free-living cetaceans to other acoustic sources,
such as seismic airguns and low-frequency tactical sonar, than MFAS.
Behavioral Responses
Southall et al. (2007) reports the results of the efforts of a
panel of experts in acoustic research from behavioral, physiological,
and physical disciplines that convened and reviewed the available
literature on marine mammal hearing and physiological and behavioral
responses to human-made sound with the goal of proposing exposure
criteria for certain effects. This peer-reviewed compilation of
literature is very valuable, though Southall et al. (2007) note that
not all data are equal, some have poor statistical power, insufficient
controls, and/or limited information on received levels, background
noise, and other potentially important contextual variables–such data
were reviewed and sometimes used for qualitative illustration but were
not included in the quantitative analysis for the criteria
recommendations. All of the studies considered, however, contain an
estimate of the received sound level when the animal exhibited the
indicated response.
In the Southall et al. (2007) publication, for the purposes of
analyzing responses of marine mammals to anthropogenic sound and
developing criteria, the authors differentiate between single pulse
sounds, multiple pulse sounds, and non-pulse sounds. MFAS/HFAS sonar is
considered a non-pulse sound. Southall et al. (2007) summarize the
studies associated with low-frequency, mid-frequency, and high-
frequency cetacean and pinniped responses to non-pulse sounds, based
strictly on received level, in Appendix C of their article
(incorporated by reference and summarized in the three paragraphs
below).
The studies that address responses of low-frequency cetaceans to
non-pulse sounds include data gathered in the field and related to
several types of sound sources (of varying similarity to MFAS/HFAS)
including: vessel noise, drilling and machinery playback, low-frequency
M-sequences (sine wave with multiple phase reversals) playback,
tactical low-frequency active sonar playback, drill ships, Acoustic
Thermometry of Ocean Climate (ATOC) source, and non-pulse playbacks.
These studies generally indicate no (or very limited) responses to
received levels in the 90 to 120 dB re: 1 [micro]Pa range and an
increasing likelihood of avoidance and other behavioral effects in the
120 to 160 dB range. As mentioned earlier, though, contextual variables
play a very important role in the reported responses and the severity
of effects are not linear when compared to received level. Also, few of
the laboratory or field datasets had common conditions, behavioral
contexts or sound sources, so it is not surprising that responses
differ.
The studies that address responses of mid-frequency cetaceans to
non-pulse sounds include data gathered both in the field and the
laboratory and related to several different sound sources (of varying
similarity to MFAS/HFAS) including: pingers, drilling playbacks, ship
and ice-breaking noise, vessel noise, Acoustic Harassment Devices
(AHDs), Acoustic Deterrent Devices (ADDs), MFAS, and non-pulse bands
and tones. Southall et al. (2007) were unable to come to a clear
conclusion regarding the results of these studies. In some cases,
animals in the field showed significant responses to received levels
between 90 and 120 dB, while in other cases these responses were not
seen in the 120 to 150 dB range. The disparity in results was likely
due to contextual variation and the differences between the results in
the field and laboratory data (animals typically responded at lower
levels in the field).
The studies that address responses of high frequency cetaceans to
non-pulse sounds include data gathered both in the field and the
laboratory and related to several different sound sources (of varying
similarity to MFAS/HFAS) including: pingers, AHDs, and various
laboratory non-pulse sounds. All of these data were collected from
harbor porpoises. Southall et al. (2007) concluded that the existing
data indicate that harbor porpoises are likely sensitive to a wide
range of anthropogenic sounds at low received levels (~ 90 to 120 dB),
at least for initial exposures. All recorded exposures above 140 dB
induced profound and sustained avoidance behavior in wild harbor
porpoises (Southall et al., 2007). Rapid habituation was noted in some
but not all studies. There is no data to indicate whether other high
frequency cetaceans are as sensitive to anthropogenic sound as harbor
porpoises are.
The studies that address the responses of pinnipeds in water to
non-pulse sounds include data gathered both in the field and the
laboratory and related to several different sound sources (of varying
similarity to MFAS/HFAS) including: AHDs, ATOC, various non-pulse
sounds used in underwater data communication; underwater drilling, and
construction noise. Few studies exist with enough information to
include them in the analysis. The limited data suggested that exposures
to non-pulse sounds between 90 and 140 dB generally do not result in
strong behavioral responses in pinnipeds in water, but no data exist at
higher received levels.
In addition to summarizing the available data, the authors of
Southall et al. (2007) developed a severity scaling system with the
intent of ultimately being able to assign some level of biological
significance to a response. Following is a summary of their scoring
system; a comprehensive list of the behaviors associated with each
score, along with the assigned scores, may be found in the report:
0-3 (Minor and/or brief behaviors) includes, but is not
limited to: no response; minor changes in speed or locomotion (but with
no avoidance); individual alert behavior; minor cessation in vocal
behavior; minor changes in response to trained behaviors (in laboratory)
4-6 (Behaviors with higher potential to affect foraging,
reproduction, or survival) includes, but is not limited to: moderate
changes in speed, direction, or dive profile; brief shift in group
distribution; prolonged cessation or modification of vocal behavior
(duration > duration of sound), minor or moderate individual and/or
group avoidance of sound; brief cessation of reproductive behavior; or
refusal to initiate trained tasks (in laboratory)
7-9 (Behaviors considered likely to affect the
aforementioned vital rates) includes, but is not limited to: extensive
or prolonged aggressive behavior; moderate, prolonged or significant
separation of females and dependent offspring with disruption of
acoustic reunion mechanisms; long-term avoidance of an area; outright
panic, stampede, stranding; threatening or attacking sound source (in
laboratory)
Potential Effects of Behavioral Disturbance
The different ways that marine mammals respond to sound are
sometimes indicators of the ultimate effect that exposure to a given
stimulus will have on the well-being (survival, reproduction, etc.) of
an animal. There is little marine mammal data quantitatively relating
the exposure of marine mammals to sound to effects on reproduction or
survival, though data exists for terrestrial species to which we can
draw comparisons for marine mammals.
Attention is the cognitive process of selectively concentrating on
one aspect of an animal’s environment while ignoring other things
(Posner, 1994). Because animals (including humans) have limited
cognitive resources, there is a limit to how much sensory information
they can process at any time. The phenomenon called “attentional
capture” occurs when a stimulus (usually a stimulus that an animal is
not concentrating on or attending to) “captures” an animal’s
attention. This shift in attention can occur consciously or
subconsciously (for example, when an animal hears sounds that it
associates with the approach of a predator) and the shift in attention
can be sudden (Dukas, 2002; van Rij, 2007). Once a stimulus has
captured an animal’s attention, the animal can respond by ignoring the
stimulus, assuming a “watch and wait” posture, or treat the stimulus
as a disturbance and respond accordingly, which includes scanning for
the source of the stimulus or “vigilance” (Cowlishaw et al., 2004).
Vigilance is normally an adaptive behavior that helps animals
determine the presence or absence of predators, assess their distance
from conspecifics, or to attend cues from prey (Bednekoff and Lima,
1998; Treves, 2000). Despite those benefits, however, vigilance has a
cost of time; when animals focus their attention on specific
environmental cues, they are not attending to other activities such as
foraging. These costs have been documented best in foraging animals,
where vigilance has been shown to substantially reduce feeding rates
(Saino, 1994; Beauchamp and Livoreil, 1997; Fritz et al., 2002).
Animals will spend more time being vigilant, which may translate to
less time foraging or resting, when disturbance stimuli approach them
more directly, remain at closer distances, have a greater group size
(for example, multiple surface vessels), or when they co-occur with
times that an animal perceives increased risk (for example, when they
are giving birth or accompanied by a calf). Most of the published
literature, however, suggests that direct approaches will increase the
amount of time animals will dedicate to being vigilant. For example,
bighorn sheep and Dall’s sheep dedicated more time being vigilant, and
less time resting or foraging, when aircraft made direct approaches
over them (Frid, 2001; Stockwell et al., 1991).
Several authors have established that long-term and intense
disturbance stimuli can cause population declines by reducing the body
condition of individuals that have been disturbed, followed by reduced
reproductive success, reduced survival, or both (Daan et al., 1996;
Madsen, 1994; White, 1983). For example, Madsen (1994) reported that
pink-footed geese in undisturbed habitat gained body mass and had about
a 46-percent reproductive success rate compared with geese in disturbed
habitat (being consistently scared off the fields on which they were
foraging) which did not gain mass and had a 17-percent reproductive
success rate. Similar reductions in reproductive success have been
reported for mule deer disturbed by all-terrain vehicles (Yarmoloy et
al., 1988), caribou disturbed by seismic exploration blasts (Bradshaw
et al., 1998), caribou disturbed by low-elevation military jet-fights
(Luick et al., 1996), and caribou disturbed by low-elevation jet
flights (Harrington and Veitch, 1992). Similarly, a study of elk that
were disturbed experimentally by pedestrians concluded that the ratio
of young to mothers was inversely related to disturbance rate (Phillips
and Alldredge, 2000).
The primary mechanism by which increased vigilance and disturbance
appear to affect the fitness of individual animals is by disrupting an
animal’s time budget and, as a result, reducing the time they might
spend foraging and resting (which increases an animal’s activity rate
and energy demand). For example, a study of grizzly bears reported that
bears disturbed by hikers reduced their energy intake by an average of
12 kcal/minute (50.2 x 103kJ/minute), and spent energy
fleeing or acting aggressively toward hikers (White et al. 1999).
Alternately, Ridgway et al., (2006) reported that increased vigilance
in bottlenose dolphins exposed to sound over a 5-day period did not
cause any sleep deprivation or stress effects such as changes in
cortisol or epinephrine levels.
On a related note, many animals perform vital functions, such as
feeding, resting, traveling, and socializing, on a diel cycle (24-hour
cycle). Substantive behavioral reactions to noise exposure (such as
disruption of critical life functions, displacement, or avoidance of
important habitat) are more likely to be significant if they last more
than one diel cycle or recur on subsequent days (Southall et al.,
2007). Consequently, a behavioral response lasting less than 1 day and
not recurring on subsequent days is not considered particularly severe
unless it could directly affect reproduction or survival (Southall et
al., 2007).
In response to the National Research Council of the National
Academies (2005) review, the Office of Naval Research founded a working
group to formalize the Population Consequences of Acoustic Disturbance
(PCAD) framework. The PCAD model connects observable data through a
series of transfer functions using a case study approach. The long-term
goal is to improve the understanding of how effects of sound on marine
mammals transfer between behavior and life functions and between life
functions and vital rates of individuals. Then, this understanding of
how disturbance can affect the vital rates of individuals will
facilitate the further assessment of the population level effects of
anthropogenic sound on marine mammals by providing a quantitative
approach to evaluate effects and the relationship between takes and
possible changes to adult survival and/or annual recruitment.
Stranding and Mortality
When a live or dead marine mammal swims or floats onto shore and
becomes
[[Page 7005]]
“beached” or incapable of returning to sea, the event is termed a
“stranding” (Geraci et al., 1999; Perrin and Geraci, 2002; Geraci and
Lounsbury, 2005; NMFS, 2007). The legal definition for a stranding
within the U.S. is that (A) “a marine mammal is dead and is (i) on a
beach or shore of the United States; or (ii) in waters under the
jurisdiction of the United States (including any navigable waters); or
(B) a marine mammal is alive and is (i) on a beach or shore of the
United States and unable to return to the water; (ii) on a beach or
shore of the United States and, although able to return to the water,
is in need of apparent medical attention; or (iii) in the waters under
the jurisdiction of the United States (including any navigable waters),
but is unable to return to its natural habitat under its own power or
without assistance.” (16 U.S.C. 1421h).
Marine mammals are known to strand for a variety of reasons, such
as infectious agents, biotoxicosis, starvation, fishery interaction,
ship strike, unusual oceanographic or weather events, sound exposure,
or combinations of these stressors sustained concurrently or in series.
However, the cause or causes of most strandings are unknown (Geraci et
al., 1976; Eaton, 1979; Odell et al., 1980; Best, 1982). Numerous
studies suggest that the physiology, behavior, habitat relationships,
age, or condition of cetaceans may cause them to strand or might
predispose them to strand when exposed to another phenomenon. These
suggestions are consistent with the conclusions of numerous other
studies that have demonstrated that combinations of dissimilar
stressors commonly combine to kill an animal or dramatically reduce its
fitness, even though one exposure without the other does not produce
the same result (Chroussos, 2000; Creel, 2005; DeVries et al., 2003;
Fair and Becker, 2000; Foley et al., 2001; Moberg, 2000; Relyea, 2005a,
2005b; Romero, 2004; Sih et al., 2004). For reference, between 2001 and
2009, there was an annual average of 1,400 cetacean strandings and
4,300 pinniped strandings along the coasts of the continental U.S. and
Alaska (NMFS, 2011).
Several sources have published lists of mass stranding events of
cetaceans in an attempt to identify relationships between those
stranding events and military sonar (Hildebrand, 2004; IWC, 2005;
Taylor et al., 2004). For example, based on a review of stranding
records between 1960 and 1995, the International Whaling Commission
(2005) identified ten mass stranding events of Cuvier’s beaked whales
had been reported and one mass stranding of four Baird’s beaked whale.
The IWC concluded that, out of eight stranding events reported from the
mid-1980s to the summer of 2003, seven had been coincident with the use
of tactical mid-frequency sonar, one of those seven had been associated
with the use of tactical low-frequency sonar, and the remaining
stranding event had been associated with the use of seismic airguns.
Most of the stranding events reviewed by the International Whaling
Commission involved beaked whales. A mass stranding of Cuvier’s beaked
whales in the eastern Mediterranean Sea occurred in 1996 (Frantzis,
1998) and mass stranding events involving Gervais’ beaked whales,
Blainville’s beaked whales, and Cuvier’s beaked whales occurred off the
coast of the Canary Islands in the late 1980s (Simmonds and Lopez-
Jurado, 1991). The stranding events that occurred in the Canary Islands
and Kyparissiakos Gulf in the late 1990s and the Bahamas in 2000 have
been the most intensively-studied mass stranding events and have been
associated with naval maneuvers involving the use of tactical sonar.
Between 1960 and 2006, 48 strandings (68 percent) involved beaked
whales, three (4 percent) involved dolphins, and 14 (20 percent)
involved whale species. Cuvier’s beaked whales were involved in the
greatest number of these events (48 or 68 percent), followed by sperm
whales (seven or 10 percent), and Blainville’s and Gervais’ beaked
whales (four each or 6 percent). Naval activities (not just activities
conducted by the U.S. Navy) that might have involved active sonar are
reported to have coincided with nine or 10 (13 to 14 percent) of those
stranding events. Between the mid-1980s and 2003 (the period reported
by the International Whaling Commission), we identified reports of 44
mass cetacean stranding events of which at least seven were coincident
with naval exercises that were using MFAS.
Strandings Associated With Impulse Sound
During a Navy training event on March 4, 2011 at the Silver Strand
Training Complex in San Diego, California, three or possibly four
dolphins were killed in an explosion. During an underwater detonation
training event, a pod of 100 to 150 long-beaked common dolphins were
observed moving toward the 700-yd (640.1-m) exclusion zone around the
explosive charge, monitored by personnel in a safety boat and
participants in a dive boat. Approximately 5 minutes remained on a
time-delay fuse connected to a single 8.76 lb (3.97 kg) explosive
charge (C-4 and detonation cord). Although the dive boat was placed
between the pod and the explosive in an effort to guide the dolphins
away from the area, that effort was unsuccessful and three long-beaked
common dolphins near the explosion died. In addition to the three
dolphins found dead on March 4, the remains of a fourth dolphin were
discovered on March 7, 2011 near Ocean Beach, California (3 days later
and approximately 11.8 mi. [19 km] from Silver Strand where the
training event occurred), which might also have been related to this
event. Association of the fourth stranding with the training event is
uncertain because dolphins strand on a regular basis in the San Diego
area. Details such as the dolphins’ depth and distance from the
explosive at the time of the detonation could not be estimated from the
250 yd (228.6 m) standoff point of the observers in the dive boat or
the safety boat.
These dolphin mortalities are the only known occurrence of a U.S.
Navy training or testing event involving impulse energy (underwater
detonation) that caused mortality or injury to a marine mammal. Despite
this being a rare occurrence, the Navy has reviewed training
requirements, safety procedures, and possible mitigation measures and
implemented changes to reduce the potential for this to occur in the
future. Discussions of procedures associated with these and other
training and testing events are presented in the Mitigation section.
Strandings Associated With MFAS
Over the past 16 years, there have been five stranding events
coincident with military mid-frequency sonar use in which exposure to
sonar is believed to have been a contributing factor: Greece (1996);
the Bahamas (2000); Madeira (2000); Canary Islands (2002); and Spain
(2006). Additionally, in 2004, during the Rim of the Pacific (RIMPAC)
exercises, between 150 and 200 usually pelagic melon-headed whales
occupied the shallow waters of Hanalei Bay, Kauai, Hawaii for over 28
hours. NMFS determined that MFAS was a plausible, if not likely,
contributing factor in what may have been a confluence of events that
led to the stranding. A number of other stranding events coincident
with the operation of mid-frequency sonar, including the death of
beaked whales or other species (minke whales, dwarf sperm whales, pilot
whales), have been reported; however, the majority have not been
investigated to the degree necessary to determine the cause of the
stranding and only one of these stranding events, the Bahamas (2000),
was associated with exercises conducted by the U.S. Navy.
Greece (1996)–Twelve Cuvier’s beaked whales stranded atypically
(in both time and space) along a 38.2-km strand of the Kyparissiakos
Gulf coast on May 12 and 13, 1996 (Frantzis, 1998). From May 11 through
May 15, the North Atlantic Treaty Organization (NATO) research vessel
Alliance was conducting sonar tests with signals of 600 Hz and 3 kHz
and source levels of 228 and 226 dB re: 1[mu]Pa, respectively (D’Amico
and Verboom, 1998; D’Spain et al., 2006). The timing and location of
the testing encompassed the time and location of the strandings
(Frantzis, 1998).
Necropsies of eight of the animals were performed but were limited
to basic external examination and sampling of stomach contents, blood,
and skin. No ears or organs were collected, and no histological samples
were preserved. No apparent abnormalities or wounds were found.
Examination of photos of the animals, taken soon after their death,
revealed that the eyes of at least four of the individuals were
bleeding. Photos were taken soon after their death (Frantzis, 2004).
Stomach contents contained the flesh of cephalopods, indicating that
feeding had recently taken place (Frantzis, 1998).
All available information regarding the conditions associated with
this stranding event were compiled, and many potential causes were
examined including major pollution events, prominent tectonic activity,
unusual physical or meteorological events, magnetic anomalies,
epizootics, and conventional military activities (International Council
for the Exploration of the Sea, 2005a). However, none of these
potential causes coincided in time or space with the mass stranding, or
could explain its characteristics (International Council for the
Exploration of the Sea, 2005a). The robust condition of the animals,
plus the recent stomach contents, is inconsistent with pathogenic
causes. In addition, environmental causes can be ruled out as there
were no unusual environmental circumstances or events before or during
this time period and within the general proximity (Frantzis, 2004).
Because of the rarity of this mass stranding of Cuvier’s beaked
whales in the Kyparissiakos Gulf (first one in history), the
probability for the two events (the military exercises and the
strandings) to coincide in time and location, while being independent
of each other, was thought to be extremely low (Frantzis, 1998).
However, because full necropsies had not been conducted, and no
abnormalities were noted, the cause of the strandings could not be
precisely determined (Cox et al., 2006). A Bioacoustics Panel convened
by NATO concluded that the evidence available did not allow them to
accept or reject sonar exposures as a causal agent in these stranding
events. The analysis of this stranding event provided support for, but
no clear evidence for, the cause-and-effect relationship of tactical
sonar training activities and beaked whale strandings (Cox et al.,
2006).
Bahamas (2000)–NMFS and the Navy prepared a joint report
addressing the multi-species stranding in the Bahamas in 2000, which
took place within 24 hours of U.S. Navy ships using MFAS as they passed
through the Northeast and Northwest Providence Channels on March 15-16,
2000. The ships, which operated both AN/SQS-53C and AN/SQS-56, moved
through the channel while emitting sonar pings approximately every 24
seconds. Of the 17 cetaceans that stranded over a 36-hr period
(Cuvier’s beaked whales, Blainville’s beaked whales, minke whales, and
a spotted dolphin), seven animals died on the beach (five Cuvier’s
beaked whales, one Blainville’s beaked whale, and the spotted dolphin),
while the other 10 were returned to the water alive (though their
ultimate fate is unknown). As discussed in the Bahamas report (DOC/DON,
2001), there is no likely association between the minke whale and
spotted dolphin strandings and the operation of MFAS.
Necropsies were performed on five of the stranded beaked whales.
All five necropsied beaked whales were in good body condition, showing
no signs of infection, disease, ship strike, blunt trauma, or fishery
related injuries, and three still had food remains in their stomachs.
Auditory structural damage was discovered in four of the whales,
specifically bloody effusions or hemorrhaging around the ears.
Bilateral intracochlear and unilateral temporal region subarachnoid
hemorrhage, with blood clots in the lateral ventricles, were found in
two of the whales. Three of the whales had small hemorrhages in their
acoustic fats (located along the jaw and in the melon).
A comprehensive investigation was conducted and all possible causes
of the stranding event were considered, whether they seemed likely at
the outset or not. Based on the way in which the strandings coincided
with ongoing naval activity involving tactical MFAS use, in terms of
both time and geography, the nature of the physiological effects
experienced by the dead animals, and the absence of any other acoustic
sources, the investigation team concluded that MFAS aboard U.S. Navy
ships that were in use during the active sonar exercise in question
were the most plausible source of this acoustic or impulse trauma to
beaked whales. This sound source was active in a complex environment
that included the presence of a surface duct, unusual and steep
bathymetry, a constricted channel with limited egress, intensive use of
multiple, active sonar units over an extended period of time, and the
presence of beaked whales that appear to be sensitive to the
frequencies produced by these active sonars. The investigation team
concluded that the cause of this stranding event was the confluence of
the Navy MFAS and these contributory factors working together, and
further recommended that the Navy avoid operating MFAS in situations
where these five factors would be likely to occur. This report does not
conclude that all five of these factors must be present for a stranding
to occur, nor that beaked whales are the only species that could
potentially be affected by the confluence of the other factors. Based
on this, NMFS believes that the operation of MFAS in situations where
surface ducts exist, or in marine environments defined by steep
bathymetry and/or constricted channels may increase the likelihood of
producing a sound field with the potential to cause cetaceans
(especially beaked whales) to strand, and therefore, suggests the need
for increased vigilance while operating MFAS in these areas, especially
when beaked whales (or potentially other deep divers) are likely
present.
Madeira, Spain (2000)–From May 10-14, 2000, three Cuvier’s beaked
whales were found atypically stranded on two islands in the Madeira
archipelago, Portugal (Cox et al., 2006). A fourth animal was reported
floating in the Madeiran waters by fisherman but did not come ashore
(Woods Hole Oceanographic Institution, 2005). Joint NATO amphibious
training peacekeeping exercises involving participants from 17
countries 80 warships, took place in Portugal during May 2-15, 2000.
The bodies of the three stranded whales were examined post mortem
(Woods Hole Oceanographic Institution, 2005), though only one of the
stranded whales was fresh enough (24 hours after stranding) to be
necropsied (Cox et al., 2006). Results from the necropsy revealed
evidence of hemorrhage and congestion in the right lung and both
kidneys (Cox et al., 2006). There was also evidence of intercochlear
and intracranial hemorrhage similar to that which was observed in the
whales that stranded in the Bahamas event (Cox et al., 2006). There were no signs
of blunt trauma, and no major fractures (Woods Hole Oceanographic
Institution, 2005).
The cranial sinuses and airways were found to be clear with little
or no fluid deposition, which may indicate good preservation of tissues
(Woods Hole Oceanographic Institution, 2005).
Several observations on the Madeira stranded beaked whales, such as
the pattern of injury to the auditory system, are the same as those
observed in the Bahamas strandings. Blood in and around the eyes,
kidney lesions, pleural hemorrhages, and congestion in the lungs are
particularly consistent with the pathologies from the whales stranded
in the Bahamas, and are consistent with stress and pressure related
trauma. The similarities in pathology and stranding patterns between
these two events suggest that a similar pressure event may have
precipitated or contributed to the strandings at both sites (Woods Hole
Oceanographic Institution, 2005).
Even though no definitive causal link can be made between the
stranding event and naval exercises, certain conditions may have
existed in the exercise area that, in their aggregate, may have
contributed to the marine mammal strandings (Freitas, 2004): exercises
were conducted in areas of at least 547 fathoms (1,000 m) depth near a
shoreline where there is a rapid change in bathymetry on the order of
547 to 3,281 fathoms (1,000 to 6,000 m) occurring across a relatively
short horizontal distance (Freitas, 2004); multiple ships were
operating around Madeira, though it is not known if MFAS was used, and
the specifics of the sound sources used are unknown (Cox et al., 2006,
Freitas, 2004); and exercises took place in an area surrounded by
landmasses separated by less than 35 nm (65 km) and at least 10 nm (19
km) in length, or in an embayment. Exercises involving multiple ships
employing MFAS near land may produce sound directed towards a channel
or embayment that may cut off the lines of egress for marine mammals
(Freitas, 2004).
Canary Islands, Spain (2002)–The southeastern area within the
Canary Islands is well known for aggregations of beaked whales due to
its ocean depths of greater than 547 fathoms (1,000 m) within a few
hundred meters of the coastline (Fernandez et al., 2005). On September
24, 2002, 14 beaked whales were found stranded on Fuerteventura and
Lanzarote Islands in the Canary Islands (International Council for
Exploration of the Sea, 2005a). Seven whales died, while the remaining
seven live whales were returned to deeper waters (Fernandez et al.,
2005). Four beaked whales were found stranded dead over the next three
days either on the coast or floating offshore. These strandings
occurred within near proximity of an international naval exercise that
utilized MFAS and involved numerous surface warships and several
submarines. Strandings began about 4 hours after the onset of MFAS
activity (International Council for Exploration of the Sea, 2005a;
Fernandez et al., 2005).
Eight Cuvier’s beaked whales, one Blainville’s beaked whale, and
one Gervais’ beaked whale were necropsied, six of them within 12 hours
of stranding (Fernandez et al., 2005). No pathogenic bacteria were
isolated from the carcasses (Jepson et al., 2003). The animals
displayed severe vascular congestion and hemorrhage especially around
the tissues in the jaw, ears, brain, and kidneys, displaying marked
disseminated microvascular hemorrhages associated with widespread fat
emboli (Jepson et al., 2003; International Council for Exploration of
the Sea, 2005a). Several organs contained intravascular bubbles,
although definitive evidence of gas embolism in vivo is difficult to
determine after death (Jepson et al., 2003). The livers of the
necropsied animals were the most consistently affected organ, which
contained macroscopic gas-filled cavities and had variable degrees of
fibrotic encapsulation. In some animals, cavitary lesions had
extensively replaced the normal tissue (Jepson et al., 2003). Stomachs
contained a large amount of fresh and undigested contents, suggesting a
rapid onset of disease and death (Fernandez et al., 2005). Head and
neck lymph nodes were enlarged and congested, and parasites were found
in the kidneys of all animals (Fernandez et al., 2005).
The association of NATO MFAS use close in space and time to the
beaked whale strandings, and the similarity between this stranding
event and previous beaked whale mass strandings coincident with sonar
use, suggests that a similar scenario and causative mechanism of
stranding may be shared between the events. Beaked whales stranded in
this event demonstrated brain and auditory system injuries,
hemorrhages, and congestion in multiple organs, similar to the
pathological findings of the Bahamas and Madeira stranding events. In
addition, the necropsy results of Canary Islands stranding event lead
to the hypothesis that the presence of disseminated and widespread gas
bubbles and fat emboli were indicative of nitrogen bubble formation,
similar to what might be expected in decompression sickness (Jepson et
al., 2003; Fern[aacute]ndez et al., 2005).
Hanalei Bay (2004)–On July 3 and 4, 2004, approximately 150 to 200
melon-headed whales occupied the shallow waters of the Hanalei Bay,
Kaua’i, Hawaii for over 28 hrs. Attendees of a canoe blessing observed
the animals entering the Bay in a single wave formation at 7 a.m. on
July 3, 2004. The animals were observed moving back into the shore from
the mouth of the Bay at 9 a.m. The usually pelagic animals milled in
the shallow bay and were returned to deeper water with human assistance
beginning at 9:30 a.m. on July 4, 2004, and were out of sight by 10:30
a.m.
Only one animal, a calf, was known to have died following this
event. The animal was noted alive and alone in the Bay on the afternoon
of July 4, 2004, and was found dead in the Bay the morning of July 5,
2004. A full necropsy, magnetic resonance imaging, and computerized
tomography examination were performed on the calf to determine the
manner and cause of death. The combination of imaging, necropsy and
histological analyses found no evidence of infectious, internal
traumatic, congenital, or toxic factors. Cause of death could not be
definitively determined, but it is likely that maternal separation,
poor nutritional condition, and dehydration contributed to the final
demise of the animal. Although we do not know when the calf was
separated from its mother, the animals’ movement into the Bay and
subsequent milling and re-grouping may have contributed to the
separation or lack of nursing, especially if the maternal bond was weak
or this was an inexperienced mother with her first calf.
Environmental factors, abiotic and biotic, were analyzed for any
anomalous occurrences that would have contributed to the animals
entering and remaining in Hanalei Bay. The Bay’s bathymetry is similar
to many other sites within the Hawaiian Island chain and dissimilar to
sites that have been associated with mass strandings in other parts of
the U.S. The weather conditions appeared to be normal for that time of
year with no fronts or other significant features noted. There was no
evidence of unusual distribution, occurrence of predator or prey
species, or unusual harmful algal blooms, although Mobley et al., 2007
suggested that the full moon cycle that occurred at that time may have
influenced a run of squid into the Bay. Weather patterns and bathymetry
that have been associated with mass strandings elsewhere were not found to occur in this instance.
The Hanalei event was spatially and temporally correlated with
RIMPAC. Official sonar training and tracking exercises in the Pacific
Missile Range Facility (PMRF) warning area did not commence until
approximately 8 a.m. on July 3 and were thus ruled out as a possible
trigger for the initial movement into the Bay. However, six naval
surface vessels transiting to the operational area on July 2
intermittently transmitted active sonar (for approximately 9 hours
total from 1:15 p.m. to 12:30 a.m.) as they approached from the south.
The potential for these transmissions to have triggered the whales’
movement into Hanalei Bay was investigated. Analyses with the
information available indicated that animals to the south and east of
Kaua’i could have detected active sonar transmissions on July 2, and
reached Hanalei Bay on or before 7 a.m. on July 3. However, data
limitations regarding the position of the whales prior to their arrival
in the Bay, the magnitude of sonar exposure, behavioral responses of
melon-headed whales to acoustic stimuli, and other possible relevant
factors preclude a conclusive finding regarding the role of sonar in
triggering this event. Propagation modeling suggests that transmissions
from sonar use during the July 3 exercise in the PMRF warning area may
have been detectable at the mouth of the Bay. If the animals responded
negatively to these signals, it may have contributed to their continued
presence in the Bay. The U.S. Navy ceased all active sonar
transmissions during exercises in this range on the afternoon of July
3. Subsequent to the cessation of sonar use, the animals were herded
out of the Bay.
While causation of this stranding event may never be unequivocally
determined, we consider the active sonar transmissions of July 2-3,
2004, a plausible, if not likely, contributing factor in what may have
been a confluence of events. This conclusion is based on the following:
(1) The evidently anomalous nature of the stranding; (2) its close
spatiotemporal correlation with wide-scale, sustained use of sonar
systems previously associated with stranding of deep-diving marine
mammals; (3) the directed movement of two groups of transmitting
vessels toward the southeast and southwest coast of Kauai; (4) the
results of acoustic propagation modeling and an analysis of possible
animal transit times to the Bay; and (5) the absence of any other
compelling causative explanation. The initiation and persistence of
this event may have resulted from an interaction of biological and
physical factors. The biological factors may have included the presence
of an apparently uncommon, deep-diving cetacean species (and possibly
an offshore, non-resident group), social interactions among the animals
before or after they entered the Bay, and/or unknown predator or prey
conditions. The physical factors may have included the presence of
nearby deep water, multiple vessels transiting in a directed manner
while transmitting active sonar over a sustained period, the presence
of surface sound ducting conditions, and/or intermittent and random
human interactions while the animals were in the Bay.
A separate event involving melon-headed whales and rough-toothed
dolphins took place over the same period of time in the Northern
Mariana Islands (Jefferson et al., 2006), which is several thousand
miles from Hawaii. Some 500 to 700 melon-headed whales came into
Sasanhaya Bay on July 4, 2004, near the island of Rota and then left of
their own accord after 5.5 hours; no known active sonar transmissions
occurred in the vicinity of that event. The Rota incident led to
scientific debate regarding what, if any, relationship the event had to
the simultaneous events in Hawaii and whether they might be related by
some common factor (e.g., there was a full moon on July 2, 2004, as
well as during other melon-headed whale strandings and nearshore
aggregations (Brownell et al., 2009; Lignon et al., 2007; Mobley et
al., 2007). Brownell et al. (2009) compared the two incidents, along
with one other stranding incident at Nuka Hiva in French Polynesia and
normal resting behaviors observed at Palmyra Island, in regard to
physical features in the areas, melon-headed whale behavior, and lunar
cycles. Brownell et al., (2009) concluded that the rapid entry of the
whales into Hanalei Bay, their movement into very shallow water far
from the 100-m contour, their milling behavior (typical pre-stranding
behavior), and their reluctance to leave the bay constituted an unusual
event that was not similar to the events that occurred at Rota (but was
similar to the events at Palmyra), which appear to be similar to
observations of melon-headed whales resting normally at Palmyra Island.
Additionally, there was no correlation between lunar cycle and the
types of behaviors observed in the Brownell et al. (2009) examples.
Spain (2006)–The Spanish Cetacean Society reported an atypical
mass stranding of four beaked whales that occurred January 26, 2006, on
the southeast coast of Spain, near Mojacar (Gulf of Vera) in the
Western Mediterranean Sea. According to the report, two of the whales
were discovered the evening of January 26 and were found to be still
alive. Two other whales were discovered during the day on January 27,
but had already died. The first three animals were located near the
town of Mojacar and the fourth animal was found dead, a few kilometers
north of the first three animals. From January 25-26, 2006, Standing
NATO Response Force Maritime Group Two (five of seven ships including
one U.S. ship under NATO Operational Control) had conducted active
sonar training against a Spanish submarine within 50 nm (93 km) of the
stranding site.
Veterinary pathologists necropsied the two male and two female
Cuvier’s beaked whales. According to the pathologists, the most likely
primary cause of this type of beaked whale mass stranding event was
anthropogenic acoustic activities, most probably anti-submarine MFAS
used during the military naval exercises. However, no positive acoustic
link was established as a direct cause of the stranding. Even though no
causal link can be made between the stranding event and naval
exercises, certain conditions may have existed in the exercise area
that, in their aggregate, may have contributed to the marine mammal
strandings (Freitas, 2004): exercises were conducted in areas of at
least 547 fathoms (1,000 m) depth near a shoreline where there is a
rapid change in bathymetry on the order of 547 to 3,281 fathoms (1,000
to 6,000 m) occurring across a relatively short horizontal distance
(Freitas, 2004); multiple ships (in this instance, five) were operating
MFAS in the same area over extended periods of time (in this case, 20
hours) in close proximity; and exercises took place in an area
surrounded by landmasses, or in an embayment. Exercises involving
multiple ships employing MFAS near land may have produced sound
directed towards a channel or embayment that may have cut off the lines
of egress for the affected marine mammals (Freitas, 2004).
Association Between Mass Stranding Events and Exposure to MFAS
Several authors have noted similarities between some of these
stranding incidents: they occurred in islands or archipelagoes with
deep water nearby, several appeared to have been associated with
acoustic waveguides like surface ducting, and the sound fields created
by ships transmitting MFAS (Cox et al., 2006, D’Spain et al., 2006).
Although Cuvier’s beaked whales have been the most common species involved in these
stranding events (81 percent of the total number of stranded animals),
other beaked whales (including Mesoplodon europeaus, M. densirostris,
and Hyperoodon ampullatus) comprise 14 percent of the total. Other
species (Stenella coeruleoalba, Kogia breviceps and Balaenoptera
acutorostrata) have stranded, but in much lower numbers and less
consistently than beaked whales.
Based on the evidence available, however, we cannot determine
whether (a) Cuvier’s beaked whale is more prone to injury from high-
intensity sound than other species; (b) their behavioral responses to
sound makes them more likely to strand; or (c) they are more likely to
be exposed to MFAS than other cetaceans (for reasons that remain
unknown). Because the association between active sonar exposures and
marine mammals mass stranding events is not consistent–some marine
mammals strand without being exposed to sonar and some sonar
transmissions are not associated with marine mammal stranding events
despite their co-occurrence–other risk factors or a grouping of risk
factors probably contribute to these stranding events.
Behaviorally Mediated Responses to MFAS That May Lead to Stranding
Although the confluence of Navy MFAS with the other contributory
factors noted in the report was identified as the cause of the 2000
Bahamas stranding event, the specific mechanisms that led to that
stranding (or the others) are not understood, and there is uncertainty
regarding the ordering of effects that led to the stranding. It is
unclear whether beaked whales were directly injured by sound (e.g.,
acoustically mediated bubble growth, as addressed above) prior to
stranding or whether a behavioral response to sound occurred that
ultimately caused the beaked whales to be injured and strand.
Although causal relationships between beaked whale stranding events
and active sonar remain unknown, several authors have hypothesized that
stranding events involving these species in the Bahamas and Canary
Islands may have been triggered when the whales changed their dive
behavior in a startled response to exposure to active sonar or to
further avoid exposure (Cox et al., 2006, Rommel et al., 2006). These
authors proposed three mechanisms by which the behavioral responses of
beaked whales upon being exposed to active sonar might result in a
stranding event. These include the following: gas bubble formation
caused by excessively fast surfacing; remaining at the surface too long
when tissues are supersaturated with nitrogen; or diving prematurely
when extended time at the surface is necessary to eliminate excess
nitrogen. More specifically, beaked whales that occur in deep waters
that are in close proximity to shallow waters (for example, the
“canyon areas” that are cited in the Bahamas stranding event; see
D’Spain and D’Amico, 2006), may respond to active sonar by swimming
into shallow waters to avoid further exposures and strand if they were
not able to swim back to deeper waters. Second, beaked whales exposed
to active sonar might alter their dive behavior. Changes in their dive
behavior might cause them to remain at the surface or at depth for
extended periods of time which could lead to hypoxia directly by
increasing their oxygen demands or indirectly by increasing their
energy expenditures (to remain at depth) and increase their oxygen
demands as a result. If beaked whales are at depth when they detect a
ping from an active sonar transmission and change their dive profile,
this could lead to the formation of significant gas bubbles, which
could damage multiple organs or interfere with normal physiological
function (Cox et al., 2006; Rommel et al., 2006; Zimmer and Tyack,
2007). Baird et al. (2005) found that slow ascent rates from deep dives
and long periods of time spent within 50 m of the surface were typical
for both Cuvier’s and Blainville’s beaked whales, the two species
involved in mass strandings related to naval sonar. These two
behavioral mechanisms may be necessary to purge excessive dissolved
nitrogen concentrated in their tissues during their frequent long dives
(Baird et al., 2005). Baird et al. (2005) further suggests that
abnormally rapid ascents or premature dives in response to high-
intensity sonar could indirectly result in physical harm to the beaked
whales, through the mechanisms described above (gas bubble formation or
non-elimination of excess nitrogen).
Because many species of marine mammals make repetitive and
prolonged dives to great depths, it has long been assumed that marine
mammals have evolved physiological mechanisms to protect against the
effects of rapid and repeated decompressions. Although several
investigators have identified physiological adaptations that may
protect marine mammals against nitrogen gas supersaturation (alveolar
collapse and elective circulation; Kooyman et al., 1972; Ridgway and
Howard, 1979), Ridgway and Howard (1979) reported that bottlenose
dolphins that were trained to dive repeatedly had muscle tissues that
were substantially supersaturated with nitrogen gas. Houser et al.
(2001) used these data to model the accumulation of nitrogen gas within
the muscle tissue of other marine mammal species and concluded that
cetaceans that dive deep and have slow ascent or descent speeds would
have tissues that are more supersaturated with nitrogen gas than other
marine mammals. Based on these data, Cox et al. (2006) hypothesized
that a critical dive sequence might make beaked whales more prone to
stranding in response to acoustic exposures. The sequence began with
(1) Very deep (to depths as deep as 2 kilometers) and long (as long as
90 minutes) foraging dives; (2) relatively slow, controlled ascents;
and (3) a series of “bounce” dives between 100 and 400 m in depth
(also see Zimmer and Tyack, 2007). They concluded that acoustic
exposures that disrupted any part of this dive sequence (for example,
causing beaked whales to spend more time at surface without the bounce
dives that are necessary to recover from the deep dive) could produce
excessive levels of nitrogen supersaturation in their tissues, leading
to gas bubble and emboli formation that produces pathologies similar to
decompression sickness.
Zimmer and Tyack (2007) modeled nitrogen tension and bubble growth
in several tissue compartments for several hypothetical dive profiles
and concluded that repetitive shallow dives (defined as a dive where
depth does not exceed the depth of alveolar collapse, approximately 72
m for Ziphius), perhaps as a consequence of an extended avoidance
reaction to sonar sound, could pose a risk for decompression sickness
and that this risk should increase with the duration of the response.
Their models also suggested that unrealistically rapid ascent rates of
ascent from normal dive behaviors are unlikely to result in
supersaturation to the extent that bubble formation would be expected.
Tyack et al. (2006) suggested that emboli observed in animals exposed
to mid-frequency range sonar (Jepson et al., 2003; Fernandez et al.,
2005) could stem from a behavioral response that involves repeated
dives shallower than the depth of lung collapse. Given that nitrogen
gas accumulation is a passive process (i.e. nitrogen is metabolically
inert), a bottlenose dolphin was trained to repetitively dive a profile
predicted to elevate nitrogen saturation to the point that nitrogen
bubble formation was predicted to occur. However, inspection of the vascular system of the
dolphin via ultrasound did not demonstrate the formation of
asymptomatic nitrogen gas bubbles (Houser et al., 2007). Baird et al.
(2008), in a beaked whale tagging study off Hawaii, showed that deep
dives are equally common during day or night, but “bounce dives” are
typically a daytime behavior, possibly associated with visual predator
avoidance. This may indicate that “bounce dives” are associated with
something other than behavioral regulation of dissolved nitrogen
levels, which would be necessary day and night.
If marine mammals respond to a Navy vessel that is transmitting
active sonar in the same way that they might respond to a predator,
their probability of flight responses should increase when they
perceive that Navy vessels are approaching them directly, because a
direct approach may convey detection and intent to capture (Burger and
Gochfeld, 1981, 1990; Cooper, 1997, 1998). The probability of flight
responses should also increase as received levels of active sonar
increase (and the ship is, therefore, closer) and as ship speeds
increase (that is, as approach speeds increase). For example, the
probability of flight responses in Dall’s sheep (Ovis dalli dalli)
(Frid 2001a, b), ringed seals (Phoca hispida) (Born et al., 1999),
Pacific brant (Branta bernic nigricans) and Canada geese (B.
Canadensis) increased as a helicopter or fixed-wing aircraft approached
groups of these animals more directly (Ward et al., 1999). Bald eagles
(Haliaeetus leucocephalus) perched on trees alongside a river were also
more likely to flee from a paddle raft when their perches were closer
to the river or were closer to the ground (Steidl and Anthony, 1996).
Despite the many theories involving bubble formation (both as a
direct cause of injury (see Acoustically Mediated Bubble Growth
Section) and an indirect cause of stranding (See Behaviorally Mediated
Bubble Growth Section), Southall et al., (2007) summarizes that there
is either scientific disagreement or a lack of information regarding
each of the following important points: (1) Received acoustical
exposure conditions for animals involved in stranding events; (2)
pathological interpretation of observed lesions in stranded marine
mammals; (3) acoustic exposure conditions required to induce such
physical trauma directly; (4) whether noise exposure may cause
behavioral reactions (such as atypical diving behavior) that
secondarily cause bubble formation and tissue damage; and (5) the
extent the post mortem artifacts introduced by decomposition before
sampling, handling, freezing, or necropsy procedures affect
interpretation of observed lesions.
Impulsive Sources
Underwater explosive detonations send a shock wave and sound energy
through the water and can release gaseous by-products, create an
oscillating bubble, or cause a plume of water to shoot up from the
water surface. The shock wave and accompanying noise are of most
concern to marine animals. Depending on the intensity of the shock wave
and size, location, and depth of the animal, an animal can be injured,
killed, suffer non-lethal physical effects, experience hearing related
effects with or without behavioral responses, or exhibit temporary
behavioral responses or tolerance from hearing the blast sound.
Generally, exposures to higher levels of impulse and pressure levels
would result in greater impacts to an individual animal.
Injuries resulting from a shock wave take place at boundaries
between tissues of different densities. Different velocities are
imparted to tissues of different densities, and this can lead to their
physical disruption. Blast effects are greatest at the gas-liquid
interface (Landsberg, 2000). Gas-containing organs, particularly the
lungs and gastrointestinal tract, are especially susceptible (Goertner,
1982; Hill, 1978; Yelverton et al., 1973). In addition, gas-containing
organs including the nasal sacs, larynx, pharynx, trachea, and lungs
may be damaged by compression/expansion caused by the oscillations of
the blast gas bubble (Reidenberg and Laitman, 2003). Intestinal walls
can bruise or rupture, with subsequent hemorrhage and escape of gut
contents into the body cavity. Less severe gastrointestinal tract
injuries include contusions, petechiae (small red or purple spots
caused by bleeding in the skin), and slight hemorrhaging (Yelverton et
al., 1973).
Because the ears are the most sensitive to pressure, they are the
organs most sensitive to injury (Ketten, 2000). Sound-related damage
associated with sound energy from detonations can be theoretically
distinct from injury from the shock wave, particularly farther from the
explosion. If a noise is audible to an animal, it has the potential to
damage the animal’s hearing by causing decreased sensitivity (Ketten,
1995). Sound-related trauma can be lethal or sublethal. Lethal impacts
are those that result in immediate death or serious debilitation in or
near an intense source and are not, technically, pure acoustic trauma
(Ketten, 1995). Sublethal impacts include hearing loss, which is caused
by exposures to perceptible sounds. Severe damage (from the shock wave)
to the ears includes tympanic membrane rupture, fracture of the
ossicles, damage to the cochlea, hemorrhage, and cerebrospinal fluid
leakage into the middle ear. Moderate injury implies partial hearing
loss due to tympanic membrane rupture and blood in the middle ear.
Permanent hearing loss also can occur when the hair cells are damaged
by one very loud event, as well as by prolonged exposure to a loud
noise or chronic exposure to noise. The level of impact from blasts
depends on both an animal’s location and, at outer zones, on its
sensitivity to the residual noise (Ketten, 1995).
There have been fewer studies addressing the behavioral effects of
explosives on marine mammals compared to MFAS/HFAS. However, though the
nature of the sound waves emitted from an explosion are different (in
shape and rise time) from MFAS/HFAS, we still anticipate the same sorts
of behavioral responses to result from repeated explosive detonations
(a smaller range of likely less severe responses (i.e., not rising to
the level of MMPA harassment) would be expected to occur as a result of
exposure to a single explosive detonation that was not powerful enough
or close enough to the animal to cause TTS or injury).
Vessel Strike
Commercial and Navy ship strikes of cetaceans can cause major
wounds, which may lead to the death of the animal. An animal at the
surface could be struck directly by a vessel, a surfacing animal could
hit the bottom of a vessel, or an animal just below the surface could
be cut by a vessel’s propeller. The severity of injuries typically
depends on the size and speed of the vessel (Knowlton and Kraus, 2001;
Laist et al., 2001; Vanderlaan and Taggart, 2007). The most vulnerable
marine mammals are those that spend extended periods of time at the
surface in order to restore oxygen levels within their tissues after
deep dives (e.g., the sperm whale). In addition, some baleen whales,
such as the North Atlantic right whale, seem generally unresponsive to
vessel sound, making them more susceptible to vessel collisions
(Nowacek et al., 2004). These species are primarily large, slow moving
whales. Smaller marine mammals (e.g., bottlenose dolphin) move quickly
through the water column and are often seen riding the bow wave of
large ships. Marine mammal responses to vessels
may include avoidance and changes in dive pattern (NRC, 2003).
An examination of all known ship strikes from all shipping sources
(civilian and military) indicates vessel speed is a principal factor in
whether a vessel strike results in death (Knowlton and Kraus, 2001;
Laist et al., 2001; Jensen and Silber, 2003; Vanderlaan and Taggart,
2007). In assessing records in which vessel speed was known, Laist et
al. (2001) found a direct relationship between the occurrence of a
whale strike and the speed of the vessel involved in the collision. The
authors concluded that most deaths occurred when a vessel was traveling
in excess of 13 knots.
Jensen and Silber (2003) detailed 292 records of known or probable
ship strikes of all large whale species from 1975 to 2002. Of these,
vessel speed at the time of collision was reported for 58 cases. Of
these cases, 39 (or 67 percent) resulted in serious injury or death (19
of those resulted in serious injury as determined by blood in the
water, propeller gashes or severed tailstock, and fractured skull, jaw,
vertebrae, hemorrhaging, massive bruising or other injuries noted
during necropsy and 20 resulted in death). Operating speeds of vessels
that struck various species of large whales ranged from 2 to 51 knots.
The majority (79 percent) of these strikes occurred at speeds of 13
knots or greater. The average speed that resulted in serious injury or
death was 18.6 knots. Pace and Silber (2005) found that the probability
of death or serious injury increased rapidly with increasing vessel
speed. Specifically, the predicted probability of serious injury or
death increased from 45 to 75 percent as vessel speed increased from 10
to 14 knots, and exceeded 90 percent at 17 knots. Higher speeds during
collisions result in greater force of impact, but higher speeds also
appear to increase the chance of severe injuries or death by pulling
whales toward the vessel. Computer simulation modeling showed that
hydrodynamic forces pulling whales toward the vessel hull increase with
increasing speed (Clyne, 1999; Knowlton et al., 1995).
The Jensen and Silber (2003) report notes that the database
represents a minimum number of collisions, because the vast majority
probably goes undetected or unreported. In contrast, Navy vessels are
likely to detect any strike that does occur, and they are required to
report all ship strikes involving marine mammals. Overall, the
percentages of Navy traffic relative to overall large shipping traffic
are very small (on the order of 2 percent).
Over a period of 20 years from 1991 to 2010 there have been a total
of 16 Navy vessel strikes in SOCAL, and five Navy vessel strikes in
HRC. Two of the five HRC Navy strikes were by smaller workboats (less
than 12 m in length), versus larger Navy ships. In terms of the 16
consecutive 5-year periods in the last 20 years, no single 5-year
period exceeded ten whales struck within SOCAL and HRC (periods from
2000-2004 and 2001-2005). For Navy vessel strikes in SOCAL, there were
six consecutive 5-year periods with six or more whales struck (1997-
2001, 1998-2002, 1999-2003, 2000-2004, 2001-2005, and 2002-2006), and
no more than three whales struck in the last 5-year period from 2006-
2010. No whales have been struck by Navy vessels in SOCAL since 2009.
For Navy vessel strikes in the HRC for the same time period, there was
one 5-year period when three whales were struck (2003-2007), seven
periods when two whales were struck, five periods when one whale was
struck, and three periods when no whales were struck. Within the data
set analyzed for HRC through 2010, no whales have been struck by a Navy
vessel since 2008.
Mitigation
In order to issue an incidental take authorization under section
101(a)(5)(A) of the MMPA, NMFS must set forth the “permissible methods
of taking pursuant to such activity, and other means of effecting the
least practicable adverse impact on such species or stock and its
habitat, paying particular attention to rookeries, mating grounds, and
areas of similar significance.” The NDAA of 2004 amended the MMPA as
it relates to military-readiness activities and the ITA process such
that “least practicable adverse impact” shall include consideration
of personnel safety, practicality of implementation, and impact on the
effectiveness of the “military readiness activity”. The training and
testing activities described in the Navy’s LOA application are
considered military readiness activities.
NMFS reviewed the proposed activities and the proposed mitigation
measures as described in the Navy’s LOA application to determine if
they would result in the least practicable adverse effect on marine
mammals, which includes a careful balancing of the likely benefit of
any particular measure to the marine mammals with the likely effect of
that measure on personnel safety, practicality of implementation, and
impact on the effectiveness of the “military-readiness activity.”
Included below are the mitigation measures the Navy proposed in their
LOA application.
