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UHM 2005, Vol. 32, No. 2 – Noise may disrupt neural activity in deep-diving cetaceans.
Sonar versus Whales: Noise may disrupt neural
activity in deep-diving cetaceans.
A. E. TALPALAR, Y. GROSSMAN
Department of Physiology, Faculty of Health Sciences, Zlotowski Center forNeuroscience, Ben-Gurion University of the Negev,
Beer-Sheva 84105, Israel
INTRODUCTION
In humans, and other terrestrial
animals, acoustic and non-acoustic detrimental
effects of noise have been described long
ago (1,2). In the recent years there is an
increase in public and expert interest in the
potential damaging consequences of acoustic
pollution to marine life. The general increase
in underwater noise and the use of sonar
(1,2) have been associated with behavioral
(3, 4) and pathological changes (5) in diving
mammalians exposed to such an environment.
Among these last, the connection established
between the use of high-intensity sonar and
the stranding and acute death of whales (6,)
is particularly striking. It has been suggested
that sonar activity per se may induce either
bubble formation similar to decompression
sickness (DCS (7)), or direct tissue disruption
in diving mammalians (8,9). This may be
true at the proximity of high intensity sonars
(10,11). But the general signs of DCS observed
in stranded cetaceans that were presumably
exposed to the mid-range sonar activity at
distance (5) suggest a behavioral cause: an
accelerated ascent from deep water after being
affected by the sonar. We postulate here novel
auditory and sensorineural mechanisms by
which sonar, and intense noise, may disrupt
the behavior of diving cetaceans. Together
with this, we also propose that the effects of
noise at frequency may be enhanced during
deep diving due to a synergistic combination
with the adaptive response of the central
nervous system (CNS) at high pressure.
Auditory Effects of High Intensity
Sound
Dolphins and whales are able to
perceive sound beyond the human hearing
range. Many species use sounds for behavioral
functions like mating (2), echolocation of
prey (
12,13,14) and orientation during diving
(15,16). The echolocation system of cetaceans
(mostly demonstrated in odontocetes), in
contrast with that of bats, lacks of automatic
gain-control on the receiver (ear). So, to
compensate for propagation loss, or to protect
the ear, cetaceans have to automatically adjust
the emission (their output vocal click signal)
as they approach the target (17). Because of
this feature, the damage inflicted by intense
noise to the ears may result in a severe
auditory threshold shift (18) and may lead to
permanent or transient hearing-impairment.
Thus, disabling the echolocation system of
the cetacean. If this happens during a deep
dive, failure of echolocation may lead to
disorientation, speeding up ascent from the
depth, and ultimately DCS. Such sensitivity
of the ear turns the cetaceans prone to the
acoustic assault. This may explain why
whales and dolphins can be more susceptible
to sonar stimuli (13) than young elephant
seals (19). A sensitive auditory system may
be the direct target of intense noise (13), but
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UHM 2005, Vol. 32, No. 2 – Noise may disrupt neural activity in deep-diving cetaceans.
136
it may also be the trigger of secondary effects
(5).
Non-auditory Effects of High
Intensity Sound
Whales and other deep-diving
mammals perform breath-hold diving with
pre-dive expiration, which is followed by
lung collapse and redistribution of blood flow.
This procedure impedes any gas exchange in
the lungs (20). Piantadosi and Thalmann (8)
argued that this diving response is enough
to avoid DCS under normal conditions.
However, if brain function is affected (see
Startle response below), the autonomic
nervous system may as well be dysfunctional,
impairing the preventive maneuvers that
impede gas diffusion during the dive response
(redistribution of pulmonary blood flow). Thus,
a static diffusion of nitrogen in supersaturated
tissues, usually affected by repetitive dives,
is a possible mechanism for vascular bubbles
formation. The crucial question is why whales
should react so abnormally, changing their
diving or decompression profile in presence
of the sonar signal? Even at low pressures
high intensity underwater noise was shown to
disturb human behavior (21). Non-auditory
effects of noise in humans involve annoyance
(22), disruption of short-term memory
acquisition and maintenance of ordered
information (23,24), disturbed auditory
verbal processing, and diminished attentional
control (25). Startle is a motor and also an
autonomic reaction to a totally unanticipated
and potentially frightening stimulus. A sudden
noise may develop a normal startle response,
but a high intensity noise may elicit severe
fear or a panic response (26). This kind of
response, involving an autonomic component,
may disrupt the regular diving response of
the cetacean. Furthermore, certain auditory
stimuli, such as noise (27) or music (28,29),
may eventually provoke epileptic seizures in
susceptible subjects.
Effects of high intensity noise may
be enhanced at high pressure because of
CNS adaptive mechanisms
Humans and experimental animals
exposed to high pressure suffer the high
pressure nervous syndrome (HPNS), which
is characterized by hyperexcitability of the
CNS. HPNS often begins with tremor and
cognitive disturbance, but also involves
autonomic reactions like nausea, vertigo,
vomiting and dizziness, and may, in extreme
cases, induce epilepsy-like seizures (30).
The normal inhibition the respiratory drive
by trigeminal and vagal nerves stimulation
was reduced, or even reversed to stimulation,
under hyperbaric conditions (31).
Development of HPNS has also been
associated with unusual discomfort and
abnormal psychological symptoms when
subjects were exposed to the clicks of an
auditory evoked potential (AEP) test (32).
Generation of late AEP waves is associated
with activation of high-level areas in the
cerebrum. Corticohippocampal areas have
been shown to participate in these phases
of the AEP (33). Some of these high-level
areas, are which when abnormally activated
by noise at atmospheric conditions, produce
the non-auditory deleterious effects of
noise. Reduction of synaptic transmission,
diminished action potentials conduction
velocity and paradoxical hyperexcitability
(34,35) are well-known phenomena in the
CNS under hyperbaric conditions. Humans,
and deep-diving animals may cope with these
effects due to certain adaptability of the CNS
at high pressure. This adaptation is which
presumably allows them to perform and carry
out relatively normal tasks at great depths. Our
recent experiments in isolated rat brain-slices
revealed at a cellular level that this adaptation
to high-pressure involves counterbalance of
high-pressure-induced synaptic depression
by increased dendritic excitability and
UHM 2005, Vol. 32, No. 2 – Noise may disrupt neural activity in deep-diving cetaceans.
137
conduction (36). But this adjustment is not
devoid of secondary effects: stimulation of
large number of cortical inputs at certain
frequencies may boost the activity patterns
in neural circuits, and even promote seizure
development (38). By this mechanism the
repetitive high-intensity noise produced by the
sonar pinging may activate more fibers under
high-pressure conditions than on surface.
Massive activation of corticohippocampal
areas will induce corresponding cognitive
and autonomic secondary responses that
may impair orientation, or maintenance of
the regular diving response of the cetacean.
Moreover, deep-diving whales seem to be the
most affected by sonars (7): the phenomenon
of massive stranding is almost exclusive
of odontocetes that use echolocation for
foraging at great depths. Within this group,
the Cuvier’s beaked whales are the most
likely to be found massively stranded.
These whales are also the deepest divers of
the group, using to submerge for more than
20 min at depths of approximately 2000 m
(37). Other beaked whales found stranded
after sonar use, such as Blainville’s and
Gervais, are also deep divers. Sperm whales,
which have the deep-diving world record,
occasionally strand, and display signs of DCS
in their bones (38). Presence of a huge mass
of undigested squid in the stomach of beaked
Cuvier whales stranded in the Canary Islands
(5) suggest that these animals were severely
disturbed by the sonar short after ingesting
their meal at great depth (39). Therefore, it
is in our opinion, reasonable to assume that
in this case whales dead by DCS due to rapid
ascent from the depth and/or dysfunction of
their physiologic diving response.
CONCLUSIONS
Intense noise affects animals at
various levels. Direct effects of noise on
matter and animal tissue are expected only in
the proximity of high intensity active sonars
(mostly low frequency sonars). The auditory
effects of intense noise may be particularly
harmful for deep-diving cetaceans because
of lack of gain-control in their ears. This
feature may lead to permanent or transient ear
damage together with secondary loss of the
echolocation function. Lack of echolocation
may be crucial for orientation, in particular
when the animal is diving at great depths.
Non-acoustic effects of noise may give rise
to an enhanced startle response leading to
disturbance in the normal behavior. A severe
startle response, possibly involving fear or
panic, may cause stranding as a flight response.
The cumulative effects of high-intensity
noise with CNS adaptation to high-pressure
seem to play a relevant role in the association
sonar use with stranding/DCS in whales.
Thus, it is possible that strong noise or sonar
signals are more prone to abnormally activate
brain areas when animals are concomitantly
exposed to high pressure at the depth of the
ocean. We propose that these phenomena may
interfere with their orientation cues, and alter
behavioral traits. In extreme cases, this could
cause the stranding of whales. Therefore, it
is necessary to encourage the study of neural
effects of sound waves on diving mammals
under various ambient pressures conditions.
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