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J. Comp. Path. 2008, Vol. 139, 24e33
Available online at
Histopathology of the Alarm Reaction
in Small Odontocetes
D. F. Cowan*,†,‡,x and B. E. Curryk
Department of Pathology, University of Texas Medical Branch, Galveston, TX, † The Marine Biomedical Institute,
University of Texas Medical Branch, Galveston, TX, ‡ Department of Marine Biology,
Texas A&M University at Galveston, TX, x Texas Marine Mammal Stranding Network, Galveston, TX and k Southwest
Fisheries Science Center, 8604 La Jolla Shores Drive, La Jolla, CA, USA
Pathological changes in the organs and tissues of beach-stranded, net-caught or captive small odontocete
cetaceans (whales and dolphins) are reported. These changes include contraction band necrosis of cardiac
and smooth muscles, smooth muscle spasm, ischemic injury to the intestinal mucosa (especially the mucosa
of the small intestine) and acute tubular necrosis (ATN) of the proximal tubules of the nephron. Spastic contraction of terminal bronchiolar muscular sphincters was also observed. The changes are consistent with multisystemic injury caused by massive release of endogenous catecholamines or vasospasm leading to ischemic
injury, followed by reperfusion and reperfusion injury. The histopathological findings suggest that the reflex
response of an odontocete to any major perceived threat (the ‘‘alarm reaction’’) is to activate the physiological
adaptations to diving or escape to an extreme or pathological level, resulting, if greatly prolonged, in widespread ischemic injury to tissues. These observations may explain why these species die abruptly from handling
or transportation and why the mortality of highly stressed beach-stranded animals is very high.
Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: alarm reaction; cetacean; histopathology; odontocete
Free-ranging odontocete cetaceans (whales and dolphins) survive in a very demanding environment.
They are creatures of the airewater interface and,
as air-breathers, are in constant danger of drowning
from the moment of birth. They are exposed to predation from sharks and other sea creatures, and a large
proportion bear scars, often very large, from shark
encounters and intra-species aggression. Even so,
cetaceans have made a very successful adaptation
and are found in all oceans. Hardy as they may be
in that environment, most species of small odontocete
whales and dolphins are very difficult to keep in
captivity and are adversely affected by handling.
Some beached individuals are reported to have died
after simply being picked up by would-be rescuers,
Correspondence to: D.F. Cowan (e-mail: [email protected]).
0021-9975/$ - see front matter
and many dolphins have died without overt injury
as a result of net encirclement in pelagic fishing
operations (Cowan and Walker, 1979). Such deaths
occurring in the absence of recognized injury have
been attributed to ‘‘stress’’. At least some of these
animals had myocardial lesions that have been attributed to catecholamine injury (Cowan and Walker,
1979; Turnbull and Cowan, 1998). Cowan et al.
(1986) found numerous small myocardial scars in
dolphins stranded on beaches in southern California,
but could not attribute them to inflammation or
coronary artery disease. Further research is required
to provide a definition of the hypothetical stress injury
in odontocetes.
This report describes the findings of necropsy
examinations of small odontocetes of many species
obtained in diverse circumstances. Histopathological
findings are interpreted in light of the highly specialized adaptations of cetaceans to diving and life in the
marine environment. Cetaceans are protected under
Ó 2008 Elsevier Ltd. All rights reserved.
Alarm Reaction in Odontocetes
the laws of most countries, and so critical experiments
to replicate lesions under controlled conditions are
unlikely to ever be performed. As a result, interpretation of these findings is based on parallel studies of
humans or laboratory animals.
Materials and Methods
Small odontocetes (n ¼ 407), primarily toothed
whales and dolphins of 20 different species were
collected over a period of 40 years. These animals
were of both sexes and ranged in age from neonatal
to 49 years as determined by examination of dentinal
growth layer groups (Hohn et al., 1989). Species of
dolphins and small whales examined included Atlantic bottlenose dolphin (Tursiops truncates), coastal
Pacific bottlenose dolphin (Tursiops aduncus), Fraser’s
dolphin (Lagenodelphis hosei), Pacific white-sided
dolphin (Lagenorhynchus obliquidens), melon-headed
whale (Peponocephala electra), spinner dolphin (Stenella
longirostris), pantropical spotted dolphin (Stenella
attenuata), striped dolphin (Stenella coeruleoalba),
rough-toothed dolphin (Steno bredanensis), North
Atlantic or long-finned pilot whale (Globicephala
melas), short-finned pilot whale (Globicephala macrorhynchus), common dolphin (Delphinus delphis), pygmy
sperm whale (Kogia breviceps), dwarf sperm whale (Kogia sima), killer whale (Orcinus orca), northern right
whale dolphin (Lissodelphis borealis), Risso’s dolphin
(Grampus griseus), Chinese humpback dolphin (Sousa
chinensis), Baird’s beaked whale (Mesoplodon europaeus)
and Dall’s porpoise (Phocoenoides dalli).
Collection areas included the Trinity Bay,
Newfoundland whale fishery (Cowan, 1966), eastern
tropical Pacific (ETP) purse-seine tuna fishery
(Cowan and Walker, 1979; Cowan and Curry,
2002), the beaches of Los Angeles and Orange
counties, California (Cowan et al., 1986). Animals
were also obtained from the Gulf coast of Texas,
collected by the Texas Marine Mammal Stranding
Network (TMMSN). These latter animals (n ¼ 129)
were collected between 1990 and 2006 and were examined by one author (DFC). The interval between
death and necropsy examination ranged from
20 min to 20 h. Two separate studies of by-catch in
the ETP were done, one in 1979, which included 68
animals, and the second in 2000e2001 (n ¼ 56
animals). By-caught animals were examined typically
within 1e2 h of death. Further contributions were
received from several marine aquaria and a variety
of individuals, and from the Cape Cod (Massachusetts) Stranding Network. All animals were collected
according to the laws of the various countries current
at the time and at the present time in the United States,
under permit from the National Marine Fisheries
service. No animals were killed for the purposes of
this study.
Autolysis is always a consideration in animals
examined several hours or more after death. Autolysis
was evaluated by initial assessment of the animal. Evidence of epidermal slippage, gas formation in tissues
and other evidence of bacterial action including
colour change and malodour were causes for rejection
from this study. Autolysis was also assessed microscopically by evaluation of postmortem bacterial overgrowth,
slough of vascular endothelium and pancreatic autodigestion. While only a few animals were considered
perfectly preserved, all included in this study had
only minor degrees of autolysis.
All hearts taken from animals in the TMMSN
(n ¼ 129) and the second ETP study (n ¼ 56) were
serially sliced in the transverse plane. The entire heart
was inspected and, in the absence of any specific
grossly recognizable abnormality, a standard slice
was selected for systematic sampling. The slice
selected was the one that represented the level of the
tip of the left anterior papillary muscle, an easily
recognized standard landmark. Heart sections
included the anterior left ventricle, lateral left ventricle, posterior left ventricle, anterior right ventricle,
lateral right ventricle, posterior right ventricle, and
septum from the standard slice, and a sample each
of left and right atria. In addition, any grossly
observed cardiac lesion was also sampled. Hearts
from all other sources (n ¼ 222) were sampled
randomly, mainly from the left ventricle, and from
recognized lesions.
All tissues were fixed in 10% neutral-buffered
formalin at ambient temperature and processed into
paraffin wax. Sections (5 mm) were stained with
haematoxylin and eosin (HE) or haematoxylin,
phloxine and safranin (HPS) trichrome.
A variety of naturally occurring disease was recognized in these animals. Examples of these included
parasitism of the brain and other organs (including
complications such as gastrointestinal perforation),
infection, lung disease, and either human-related
trauma such as boat strikes or entanglement in fishing
gear, or natural trauma such as caused by interspecific or intra-specific aggression. Because no differential correlations were found, except to note the
great variation in these causes, naturally occurring
disease will not be discussed further. Clark et al.
(2006) reported adrenal changes in Atlantic bottlenose dolphins from the TMMSN collections that
were deemed to be suffering from chronic stress.
D.F. Cowan and B.E. Curry
Particular acute microscopical changes were very
consistently identified in tissues from this series of animals, whatever the disease or circumstance associated
with their death. These findings were widespread,
involving many organs, but the major changes involved the myocardium. Frequent blotchy mottling
of the heart with areas of pallor alternating with areas
of congestion were interpreted to represent circulatory disturbance. Occasional subendocardial necrosis was recognized grossly (Fig. 1). Almost universal
microscopical changes in myocardial tissue included
hyperacidophilic fibres (Fig. 2), wavy fibres (Fig. 3),
perinuclear vacuolation and contraction band necrosis (Fig. 4). These changes were widespread, but they
occurred with greatest intensity in the subepicardial
and subendocardial regions of the ventricles (especially the right ventricle) and affected both atria, particularly the right atrium. Similar findings were found
in the fibres of the myocardial conduction system
(Fig. 5). The distribution of these lesions did not appear to vary with species; however, there were species
differences in the severity of these changes. Acute myocardial injury was most pronounced in Kogia, while
scarring was most prominent in Delphinus. Extramural
coronary arteries were uniformly normal, except for
the rare occurrence of small, flat, fibrous plaques. Inflammation consistent with infectious myocarditis was
observed in only one case.
In addition to the range of myocardial changes
described above, cellular disarray, vacuolation and
contraction banding were identified in the smooth
muscle of intramural coronary arteries (Fig. 6) and,
in a subset of animals, eccentric plaque formation
was noted in the intima of very small intramural
Fig. 1. Heart of a melon-headed whale showing subendocardial
pallor associated with severe ischemic injury. The right
ventricle is extensively affected, but the lesion is most
obvious as the yellowish subendocardial zone of the left
Fig. 2. Left ventricular myocardium from a spotted dolphin. The
dark fibres are dense and hyalinized. This injury more often
involves individual fibres than fascicles. Arrows indicate
representative hyalinized fibres. HPS.
arteries (Fig. 7). In addition to these features, hyalinization and disarray of arterial smooth muscle were
present and these changes were interpreted to suggest
prolonged spasm. Fibrous plaques affecting the
intima of small intramural coronary arteries were
commonly observed and these were interpreted as
being a sequela to arterial thrombosis. One animal
had evidence of recanalization of a thrombus (Fig. 8).
Many animals had evidence of ventricular myocardial scarring, and this lesion was particularly noted in
common dolphins stranded on beaches in southern
California (Cowan et al., 1986). These regions of scarring appeared as small, superficial indentations and as
stellate myocardial scars. The ventricular lesions were
sometimes accompanied by focal or diffuse atrial
Fig. 3. Left ventricular myocardium from a spotted dolphin. The
dark staining, stretched, compressed wavy fibres also have
condensed nuclei. HPS.
Alarm Reaction in Odontocetes
Fig. 4. Right ventricular myocardium from a striped dolphin
showing prominent contraction banding. Arrows indicate
representative bands which may be narrow or broad. HPS.
Fig. 6. Intramural coronary artery within the left ventricle of
a striped dolphin. There is disarray, spastic contraction
and vacuolation of mural myocytes in the vessel in the centre of the image. HPS.
fibrosis, and one 27-year-old female bottlenose dolphin from Texas had almost complete replacement
of the right atrium with fibrous scar in addition to
atrial thrombosis. Small patchy fibrous scars in the
myocardium (ventricular or atrial), of a size and in locations consistent with myocardial necrosis, as described above (Fig. 9), were common (e.g. these
were present in 20 of 56 animals in the second ETP
study). Most of these scars were small (1e2 mm),
but some were evident on gross inspection.
Contraction banding of smooth muscle of the
viscera (intestine, urinary bladder) and of the media of vessels of many organs was present in every
animal (Fig. 10). In the viscera, smooth muscle
banding was circumferential, and occasionally
produced thickening of segments of the muscularis
mucosa. Sloughing of the superficial mucosa of the
intestine was present in every case, even in animals
examined less than 1 h after death. This was most
pronounced in, but not limited to, the small
Marked contraction of the bronchial sphincter
muscles and pulmonary air entrapment was an almost
universal change (Fig. 11). This change appeared to
result in inability of the elastic lung tissue to collapse
when the thorax was opened and, in life, probably
resulted in impaired ventilation. Acute necrosis of
segments of the renal tubules (acute tubular necrosis;
ATN), commonly with infraglomerular reflux
(Fig. 12), was very common finding, present in nearly
Fig. 5. Right ventricular subendocardium from a bottlenose dolphin showing contraction banding in prominent Purkinje
fibres (arrows). Bands are broader than in the myocardium. HPS.
Fig. 7. Intramural coronary artery within the left ventricle of
a common dolphin. There is a subocclusive eccentric fibromuscular plaque, attributed to organized thrombosis.
D.F. Cowan and B.E. Curry
Fig. 8. Vascular webs (arrows) in a small intramural artery within
the left ventricle of a bottlenose dolphin. HPS.
all animals. Residue of smooth muscle injury (scarring) in the viscera was not identified.
A single definition of ‘‘stress’’ has not been generally
accepted by workers in the field of stress research
(Levine, 1985; Moberg, 1987; Chrousos et al., 1988;
Levine and Ursin, 1991; Fowler, 1995). Here, we
define the term stress as demand for adaptation with
the recognition that organisms are in a constant
condition of adjustment of physiological systems to
maintain homeostasis. Stress is then specified in terms
of the demand (‘‘stressor’’) applied. Examples of
stressors include heat stress, cold stress, crowding
stress and social interaction. In cetaceans, stress also
occurs in the adaptations needed to adjust to diving,
Fig. 9. Left ventricular myocardium from a bottlenose dolphin
showing irregular patchy fibrous scars and scattered hyalinized fibres. Note the absence of an inflammatory
infiltrate. HPS.
Fig. 10. Small intestinal muscularis propria from a spotted dolphin. There is marked contraction banding, seen here as
‘‘tiger striping’’ typically involving groups of fibres. HPS.
for flight from predators or from intraspecific aggression, or to catch prey. Stress may occur whenever
a wild animal is restrained or enclosed, however loose
the restraint or enclosure might seem to the captor.
Apprehension may be a mild psychological stressor
that may intensify to become anxiety, fright or even
terror (Fowler, 1995). Thus, the issue is not whether
cetaceans are ‘‘under stress’’ in a given situation, as
they are always under demand for adaptation. The
issue is whether the degree and duration of stress experienced is physiologically damaging or not.
The effects of stress are expected to vary with the
adaptive mechanisms of the subject, and will therefore vary with the species and its environment. Since
stress may have a psychological component, which
could be influenced by experience, it may be expected
Fig. 11. Lung from a spotted dolphin showing spasm of bronchiolar sphincters with air-trapping. S, sphincter muscle; L,
bronchial lumen; C, bronchial cartilage. HPS.
Alarm Reaction in Odontocetes
Fig. 12. Acute renal tubular necrosis in a bottlenose dolphin.
There is reflux of the detached proximal tubular epithelium into Bowman’s space of the glomerulus. G, glomerulus; TE, refluxed tubular epithelium. Arrows indicate
Bowman’s capsule. HPS.
to vary among individuals of the same species. Stress is
not imposed, but is an expression of a response to
a challenge, or stressor. Unfamiliar or extreme challenges may evoke unusual or extreme responses.
That is, damaging stress might result from inappropriate or extreme adaptive responses. Syncope, for
example, a transient dysfunction of the autonomic
nervous system, has no particular adaptive value,
but it does occur in some people under stress. In an
extreme situation, some animals undergo an extreme,
fatal cholinergic bradycardia (Fowler, 1995).
All stressors do not elicit the same physiological or
behavioural responses in all animal species. There
are different types and degrees of stress, and these
factors can influence an individual’s response to stress.
Acute stress is sudden, whereas chronic stress is
marked by long duration or frequent occurrence.
An acute stressor may elicit an adaptive physiological
response, but chronic stress may be pathogenic,
resulting in tissue changes (Clark et al., 2006). The
effects of both can be cumulative over time (Chrousos
and Gold, 1992).
Cetaceans exhibit the basic mammalian response to
stress (Curry, 1999). Chronic stress or repeated acute
stress can have maladaptive effects on immune responses, reproductive function and growth (Moberg,
1987, 1991; Rivier and Rivest, 1991; Chrousos, 1992;
Chrousos and Gold, 1992; Chrousos, 1995; McEwen
et al., 1997). Well-documented physiological responses
to stressors in odontocetes include adrenocortical
responses and effects on thyroid hormone balance.
Elevated blood cortisol levels have been observed in
odontocetes subjected to stressors such as capture,
handling and restraint, although the elevations
appear to be modest in comparison with those known
for other mammals experiencing similar stressors
(Thomson and Geraci, 1986; St Aubin and Geraci,
1990). In contrast, aldosterone, which does not typically characterize the adrenal response to stress in
terrestrial mammals, is greatly increased in cetaceans
(and pinnipeds) subjected to adrenocortical stimulation (Thomson and Geraci, 1986; St Aubin and
Geraci, 1990). This may be an adaptation reflecting
the need to enhance water and sodium reabsorption
during stress (St Aubin and Geraci, 1990; St Aubin
et al., 1996). Clark et al. (2006) have demonstrated
changes in the adrenal medulla of bottlenose dolphins
under chronic stress. Thyroid hormone balance in
odontocetes also appears to be sensitive to stress
(Ridgway and Patton, 1971; St Aubin and Geraci,
1988, 1992; Orlov et al., 1988; St Aubin et al., 1996).
Cowan and Walker (1979) in a study of by-catch
from the ETP fishery concluded that several dolphins
apparently died of massive cardiac reaction to stress,
finding cardiac lesions consistent with those produced
in laboratory animals injected with catecholamine
and humans thought to have died of stress cardiomyopathy (Cebelin and Hirsch, 1980)
The physiological response of marine mammals to
exercise is quite different from the mammalian exercise response. When terrestrial mammals, who have
unlimited access to atmospheric oxygen, undertake
exercise, ventilation rate and cardiac output increase
and peripheral vasodilation increases skeletal muscle
perfusion and the dissipation of heat through the
skin or lungs by panting. In contrast, diving marine
mammals breath-hold, the heart rate slows and peripheral vessels constrict, the degree of bradycardia
and peripheral vasoconstriction reflecting the level
of exertion. Peripheral vasoconstriction maintains
central arterial pressure despite decreased cardiac
output by reducing flow to all organs and tissues
except the brain, and all organs and tissues, including
the heart, kidneys and splanchnic organs, experience
a reduction in convective oxygen delivery resulting
from both hypoxic hypoxia and ischemic hypoxia
(Butler and Jones, 1997; Davis and Kanatous, 1999;
Kanatous et al., 1999).
An odontocete in free dive (voluntary dive) undergoes certain physiological adjustments reflecting
exercise, including reflexive apnoea, with voluntary
override, minimal cardiovascular adjustments, and
a general maintenance of aerobic metabolism (Butler
and Jones, 1997). Blood flow is reduced to the gut and
kidneys, but maintained in the heart, brain and, to
a degree, exercising muscles. The animal is able to
surface and dive repeatedly (foraging dive pattern),
as there is little lactic acid build-up. These features
have together been termed the ‘‘dive response’’. An
D.F. Cowan and B.E. Curry
odontocete in an involuntary dive situation undergoes
a somewhat different set of adjustments, which have
been termed the ‘‘dive reflex’’, but which may better
be termed an ‘‘alarm reaction’’. These adjustments
include not only reflexive apnoea, but also decreased
heart rate (diving bradycardia), reduction of cardiac
output and vasoconstriction with markedly decreased
perfusion of gut, liver, kidneys and skeletal muscle
and a substantial increase in production of lactic
acid in these tissues, which is reflected in marked
rise in blood levels on surfacing (Butler, 1982; Ridgway, 1986). The clear implication of the distinctive
reactions to voluntary and involuntary diving is
that the odontocete is responding to the environment
as it is perceived; the triggering of the alarm reaction
is a reaction to a situation interpreted by the animal as
a dire threat, and the response involves a marked autonomic reaction. Since the major threats to an
aquatic, air breathing mammal are drowning and
predation, the alarm reaction is an accentuation of
the physiological dive and escape responses.
In responding to a perceived threat, odontocetes
will mobilize for fight or flight, according to the established concept of stress. In terrestrial mammals, flight
means acceleration of muscular activity, elevation of
blood pressure, tachycardia and hyperventilation.
For a diving mammal, however, mobilization for
flight means breath-holding and re-directing the
flow of blood away from non-vital to vital oxygendependent organs (i.e. the brain and heart). This is
physiological and non-injurious, provided the
changes are coherent and not extreme or overly
protracted. Our hypothesis is that in the instance of
a novel threat perceived as extreme, the smooth coordination of the cardiovascular adjustments may break
down and a massive release of adrenergic hormone
from the adrenal medulla occurs, a phenomenon
well recognized in man and other mammals (Eliot
et al., 1977). In this instance, a ‘‘sympathetic storm’’
occurs, with spasm of small intramural coronary
arteries and myocardial ischemia, as occurs in human
drowning (Lunt and Rose, 1987) This ischemia may
be associated with arrhythmia and death of the
animal. It may result in patchy death of myocytes
followed by scarring in survivors, or it may occur
with no evidence of residual injury.
Muscle cells can respond to injury in limited fashion, so specific changes may have any of several different causes. ‘‘Wavy fibre’’ refers to a change in the
appearance of a myocardial fibre in which it becomes
thin and attenuated, dense or hyalinized, and assumes
an angulated or ‘‘wavy’’ accordion-pleated appearance as if it is longer than the space in which it is
contained, and is longitudinally compressed until it
buckles. Wavy fibres are a characteristic sign of acute
myocardial ischemia (Bouchardy and Majno, 1971,
1974; Eichbaum, 1975). Waving is thought to occur
when a fibre becomes ischemic or suffers acute adrenergic injury with impairment of electrogenesis; that is,
the fibre, while living, becomes unable to contract.
Stretching forces in diastole or stretching due to bulging of the myocardial wall stretches or attenuates the
fibres, which because unable to contract and become
longitudinally compressed as surrounding muscle
fibres or connective tissue elements shorten. The
overextended fibre is unable to contract to a normal
length relative to the fibres or tissue around it (Eichbaum, 1975). Ischemic wavy fibres are not necessarily
necrotic, although they may well become so.
Contraction banding is a manifestation of disruptive spastic contraction of contractile elements in
a myocyte and in conduction fibres, producing a characteristic coarse cross-banding of the affected fibre
(Hansen, 1995).
The lesions of the myocardium described in the
present report are all recognized to occur in man,
monkeys, rats and pigs. All are attributable to catecholamine injury (Reichenbach and Benditt, 1970;
Cebelin and Hirsch, 1980; Turnbull and Cowan,
1998), or to ischemia (Mukherjee et al., 1982; Muntz
et al., 1984). Indeed, the final effector in ischemia may
be the local release of catecholamines from the nerves
in the heart (Mukherjee et al., 1982). The lesions of the
intramural coronary vessels suggest spasm, which can
produce ischemic injury with or without necrosis
(Maseri and Chierchia, 1982), or by reperfusion,
that is, interruption of blood flow followed after an
interval by re-establishment of flow (Hansen, 1995).
The patchy discoloration of the hearts observed on
gross examination strongly suggests alternating areas
of congestion and ischemia, which may be explained
by irregular perfusion.
Healing of injured striated muscle, including myocardium, may occur without scarring provided that
the fine structure of the tissue, including basement
membranes, is intact and if nuclei survive the injury.
Therefore, the absence of recognizable scarring does
not preclude prior myocardial necrosis. Scars indicate
injury in foci too large to be amenable to restoration
(Carlson, 1973). It is worth emphasizing that myocardial injury related to ‘‘stress’’ is not limited to
odontocetes, but can occur in many species, under
both stringent artificial laboratory conditions and under natural conditions (Van Vleet and Ferrans,
Almost all animals in this study had lesions of acute
renal tubular necrosis. This lesion is most commonly
caused by prolonged renal ischemia (Kaufman et al.,
1991; Kashgarian, 1998). Infraglomerular tubular reflux is the movement or intrusion of detached
Alarm Reaction in Odontocetes
proximal tubular epithelium into Bowman’s space,
around the renal glomerulus. This change is considered a very sensitive indicator of tubular epithelial
damage (Waugh et al., 1964; Kashgarian, 1998).
ATN, as seen in odontocetes in the ETP studies, is
consistent with the histological observations of tissues
from mammals suffering from capture myopathy
(Curry, 1999).
The distal airways of cetaceans are different from
those of terrestrial animals in that the walls are
made rigid with cartilage bars to the mouth of the
alveolar duct, and the airways are equipped with
a series of muscular sphincters. Many of the odontocetes in the present study showed expansion or overexpansion of alveolar spaces, when the normal elasticity of the lung should have caused collapse on opening
the chest cavities. This was attributed to a readily
observable spasm of the sphincter muscles of the distal
airways. These smooth muscle structures also showed
overcontraction, very similar to the overcontraction
of the small intramural coronary arteries. We are
inclined to attribute this highly stereotyped multisystem pattern of smooth muscle spasm of arterial
media, bronchial sphincters and visceral smooth muscle to a single cause, massive protracted autonomic
discharge, a ‘‘sympathetic storm’’ that is accompanied by high levels of circulating catecholamines.
This discharge occurs as the major manifestation of
an extreme stress response in odontocetes.
Capture myopathy, a condition resulting from
muscle exertion associated with capture and restraint
of wildlife, is characterized by a variable and lengthy
list of clinical signs, including ataxia, paralysis,
myoglobinuria and acute muscle degeneration
(Harthoorn and Young, 1974; Bartsch et al., 1977;
Chalmers and Barrett, 1977; Basson and Hofmeyr,
1978; Hulland, 1985). Capture myopathy can be
induced by a combination of many stressors (e.g.
terror, chase, capture or restraint), and is associated
with exhaustion of the normal physiological reserves
that provide energy for escape. ATN and severe
glomerular damage have been identified in many animals dying with capture myopathy, and are considered to be the result of renal hypoxia caused by
catecholamine activity related to shock or the sympathetic storm described above (Wallace et al., 1987;
Spraker, 1993; Williams and Thorne, 1996). Myoglobinuric casts that could result from myopathy were not
found in the renal tubules of cetaceans in the present
study. While the lesions described in odontocetes in
the present study have certain features in common
with capture myopathy (myocardial lesions, ATN), systematic muscle sampling was not part of the necropsy
protocol, and we cannot assert that the alarm reaction
in cetaceans is a form of capture myopathy at this time.
The present study of many species of beachstranded, net-caught and captive odontocetes has
revealed similar patterns of pathological change in
organs and tissues. These changes are consistent
with multi-systemic injury caused by massive release
of endogenous catecholamines (alarm reaction) or
by vasospasm, including spasm of small cardiac
arteries, with ischemia and reperfusion. This pattern
of pathology includes contraction band necrosis of
cardiac and smooth muscles, ischemic injury to the
intestinal mucosa, acute renal tubular necrosis and
distal bronchospasm. The pattern appears to result
from a stereotypic stress response, independent of
the nature of the provoking stimulus. It may explain
the propensity of otherwise hardy animals to die in
an otherwise non-damaging stressful situation.
This pattern of injury is rooted in the physiological
adaptations of cetaceans that are associated with
a fully aquatic life. Histopathological findings suggest
that the reflexive response of an odontocete to any
major perceived threat, the alarm reaction, is to activate all of the physiological adaptations to diving or
escape to an extreme or pathological level, resulting,
if greatly prolonged, in widespread ischemic injury
to tissues. These observations may explain why
‘‘sensitive’’ species die abruptly from handling or
transportation, and why the mortality of highly
stressed beach-stranded animals is very high.
Thanks to Graham Worthy, past Director of
TMMSN, the volunteers of the Texas Marine Mammal Stranding Network for their enthusiastic participation, and many other contributing colleagues. This
work was supported by grants from the National
Oceanic and Atmospheric Administration (NOAA)
through the National Sea Grant College Program
(NA16RGO457-01) and the Environmental Protection Agency (EPA) Gulf of Mexico Program
(MX822147-01-0). The views expressed herein are
those of the authors and do not necessarily reflect
the views of NOAA, the EPA or any of their subagencies.
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April 12th, 2007
½ Received,
Accepted, November 22nd, 2007