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Kreuder Et Al 2001

Created By: Jessica Khalili
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http://www.jwildlifedis.org/content/39/3/495.long

ABSTRACT[1] Detailed postmortem examination of southern sea otters (Enhydra lutris nereis)
found along the California (USA) coast has provided an exceptional opportunity to understand
factors influencing survival in this threatened marine mammal species.
In order to evaluate recent
trends in causes of mortality, the demographic and geographic distribution of causes of death in
freshly deceased beachcast sea otters necropsied from 1998–2001 were evaluated. Protozoal encephalitis,
acanthocephalan-related disease, shark attack, and cardiac disease were identified as
common causes of death in sea otters examined. While infection with acanthocephalan parasites
was more likely to cause death in juvenile otters, Toxoplasma gondii encephalitis, shark attack,
and cardiac disease were more common in prime-aged adult otters. Cardiac disease is a newly
recognized cause of mortality in sea otters and T. gondii encephalitis was significantly associated
with this condition. Otters with fatal shark bites were over three times more likely to have preexisting
T. gondii encephalitis suggesting that shark attack, which is a long-recognized source of
mortality in otters, may be coupled with a recently recognized disease in otters. Spatial clusters
of cause-specific mortality were detected for T. gondii encephalitis (in Estero Bay), acanthocephalan
peritonitis (in southern Monterey Bay), and shark attack (from Santa Cruz to Point An˜ o
Nuevo). Diseases caused by parasites, bacteria, or fungi and diseases without a specified etiology
were the primary cause of death in 63.8% of otters examined. Parasitic disease alone caused
death in 38.1% of otters examined. This pattern of mortality, observed predominantly in juvenile
and prime-aged adult southern sea otters, has negative implications for the overall health and
recovery of this population.
Key words: Acanthocephalan, cardiac disease, Enhydra lutris nereis, Sarcocystis neurona,
shark predation, southern sea otter, Toxoplasma gondii.

INTRODUCTION

Evidence linking anthropogenic stressors
to unusual patterns of disease and mortality
in marine mammals has accumulated
over the past decade (Ross et al., 1996;
Harvell et al., 1999; Fair and Becker, 2000;
Daszak et al., 2001). Habitat degradation,
pollutants, municipal runoff, global climate
change, and overharvest of marine
resources are likely to have complex effects
that both directly and indirectly affect
marine mammal health. [2] Southern sea
otters (Enhyrda lutris nereis) are a useful
indicator of near-shore marine ecosystem
health because they are heavily exposed to
human activity in coastal California (USA)
and they commonly remain in one geographically
localized area for most of their
lives.
Despite legal protection since 1911
and unlike sympatric California sea lions
(Zalophus californianus), northern elephant
seals (Mirounga angustirostris), and
harbor seals (Phoca vitulina) in California
(Carretta et al., 2001), southern sea otters
have made a slower than expected recovery
after hunting drastically reduced their
numbers prior to the 20th century (Estes,
1990). Annual counts of sea otters over
their entire range in California have declined
since 1995 with the current count
at slightly over 2,000 animals (U.S. Geological
Survey, unpubl. data). Birth rates in
California sea otters appear similar to
those observed in other, rapidly growing
otter populations (Riedman et al., 1994;
Monson et al., 2000), suggesting that increased
mortality may be causing the slow
recovery rate in the California population.
A high percent of mortality due to infectious
disease was detected in detailed
necropsies of southern sea otters from 1992–95, which raised concern over the
general susceptibility of this species to infection
and subsequent mortality (Thomas
and Cole, 1996). Furthermore, some diseases
were newly recognized as important
causes of mortality in sea otters, and several
pathogens were implicated that were
not expected to cause considerable mortality
in a free-ranging marine wildlife species,
such as protozoal encephalitis, acanthocephalan
peritonitis, and coccidioidomycosis
(Thomas and Cole, 1996). Continued
monitoring of these newly recognized
diseases in sea otters is essential, not only
in light of the recent population decline,
but also because techniques used to diagnose
causes of death in sea otters have improved
with time. Furthermore, detailed
evaluation of specific patterns of mortality
in sea otters may have broad implications
for overall ecosystem health and may improve
our understanding of the processes
that promote disease in a marine mammal
population. In order to evaluate the recent
pattern of mortality in sea otters, the demographic
and geographic distribution of
causes of death for freshly deceased sea
otters found along the California coast between
1998 and 2001 were evaluated.
 
MATERIALS AND METHODS

Carcass collection and evaluation
Sea otter carcasses were recovered through
a large-scale stranding network conducted by
the California Department of Fish and Game
(CDFG), the United States Geological Survey
(USGS), the Monterey Bay Aquarium (MBA),
and The Marine Mammal Center (TMMC).
Collaborating veterinary pathologists at
CDFG’s Marine Wildlife Veterinary Care and
Research Center (MWVCRC, Santa Cruz, California)
and the University of California (UC)
School of Veterinary Medicine (Davis, California)
examined three of four freshly dead otters;
every fourth carcass was sent to the National
Wildlife Health Center (Madison, Wisconsin,
USA). Necropsy findings from otters examined
at MWVCRC/UC from February 1998 through
June 2001 were included in these analyses.
Stranding location for all otters was determined
at the time of carcass recovery. Otters
were assigned the corresponding latitude and
longitude value of their stranding location to
the nearest 0.5 km increment along a smoothed
California coastline. Stranding locations were
also categorized as north or south based on
their relation to Cape San Martin (358899N,
1218469W), which is at the center of the southern
sea otter range. Age class was determined
at necropsy and was estimated as follows: juveniles—
milk teeth present (younger than 1
yr), subadults—unworn adult dentition (approximately
1–3 yr old), prime-aged adults—
adult dentition with evidence of some tooth
wear (approximately 4–9 yr old), and aged
adults—marked tooth wear (approximately 10
yr and older). When evaluating age as a risk
factor for specific causes of death, age classes
were collapsed into a juvenile category (juveniles
and subadults) and an adult category
(prime-aged adults and aged adults). Pregnancy
and lactation status were recorded for females
at necropsy.
Only otters that were in good postmortem
condition (dead for ,4 days) were included in
this study. Otters heavily scavenged prior to
necropsy and those with incomplete histopathology
were excluded. For otters that stranded
alive but were subsequently euthanized or died
while undergoing rehabilitation, the pathologic
conditions that were the likely cause of stranding
were reported. Otters that remained in rehabilitation
for longer than 4 wk were excluded.
All otters received a complete gross necropsy,
as well as microscopic examination of
major tissues including heart, lung, liver, kidney,
spleen, stomach, small intestine, colon,
omentum, multiple lymph nodes, skeletal muscle,
spinal cord, and brain. Tissue sections were
placed in 10% neutral buffered formalin, paraffin-
embedded, sectioned at 5 mm, and stained
with hematoxylin and eosin for examination by
light microscopy. Acanthocephalan parasites
known to infect sea otters (Hennessy and Morejohn,
1977) were identified to genus by overall
size and proboscis morphology at gross necropsy
(Amin, 1992). Laboratory evaluation of
bacterial, fungal, and parasite samples and toxicologic
screening for domoic acid were performed
when indicated. Swabs for bacterial
culture were collected from heart, blood, intestinal
tract, and lung, plated on tryptic soy
agar with 5% sheep blood, MacConkey agar,
and XLT-4 agar (Hardy Diagnostics, Santa Maria,
California). Plates were incubated at 37 C.
Bacterial isolates were identified by the Microbiology
Laboratory at the UC Veterinary Medical
Teaching Hospital (Davis, California) using
standard biochemical and molecular techniques.
Tissues swabs collected from necropsied
otters with suspected fungal infections
were also submitted to the Microbiology Laboratory.
Samples were placed on wet mounts for the direct observation of spherules. Samples
were also cultured on inhibitory mold agar with
chloramphenicol (Hardy Diagnostics) and incubated
at 30 C in air for 3 wk. If fungal growth
occurred, gross colonial morphology was evaluated
and a lactophenol cotton blue preparation
(Hardy Diagnostics) was made for microscopic
examination of arthroconidia for the
identification of Coccidioides immitis (St Germain
and Summerbell, 1996). Suspect C. immitis
positive cultures were submitted to a specialty
laboratory for confirmation (D. Pappagianis,
Microbiology and Immunology, UC Davis
School of Medicine, Davis, California). On
histopathology, C. immitis was identified by the
presence of round (5–50 mm in diameter),
thick-walled spherules containing endospores.
Death was attributed to domoic acid intoxication
when substantially elevated levels of domoic
acid were detected in urine (Scholin et
al., 2000) and gross or histologic lesions suggestive
of another cause of mortality were absent.
Domoic acid was initially detected by receptor-
binding assay (Dr. Vera Trainer, National
Oceanic and Atmospheric Administration,
Northwest Fisheries Science Center, Environmental
Conservation Division, Marine Biotoxin
Program, Seattle, Washington, USA) and, when
possible, results were confirmed by liquid chromatography-
tandem mass spectroscopy (Dr.
Francis Van Dolah, National Oceanic Atmospheric
Administration, Center for Coastal Environmental
Health and Biomolecular Research,
Marine Biotoxin Program, Charleston,
South Carolina, USA).
Encephalitis was determined to be a primary
cause of death when moderate to severe inflammation
of the cerebral and/or cerebellar
neuropil was present on histopathology (Fig.
1a). This criterion was chosen because moderate
encephalitis was identified histologically in
otters undergoing rehabilitation with recurrent
seizures and severe neurologic dysfunction.
Protozoal infection with either Toxoplasma
gondii or Sarcocystis neurona was determined
to be the cause of encephalitis when protozoal
stages were directly visualized within inflammatory
foci in the neuropil on histopathology
(Fig. 1) and/or when laboratory tests confirmed
infection through isolation of protozoa from
brain tissue (Miller et al., 2001b). Antibody titers
to T. gondii and S. neurona were not used
to diagnose these parasites as the cause of encephalitis
because positive titers do not distinguish
between past exposure and active infection.
Otters with encephalitis but without histopathologic
or laboratory confirmation of protozoal
infection were diagnosed with encephalitis
of unconfirmed cause.
Trauma noted at necropsy was attributed to
shark attack when shark tooth fragments were
recovered from wounds or when multiple stablike
lacerations in soft tissue or scratches, characteristic
of contact with serrated shark teeth,
were detected on underlying bone or cartilage
(Ames and Morejohn, 1980) (Fig. 2). Similarly,
trauma was attributed to boat strike in cases
with soft tissue lacerations and fractures or cuts
in underlying bone in a pattern consistent with
a propeller injury (Ames and Morejohn, 1980).
Severe blunt trauma suggestive of a high speed
collision with a boat hull was also attributed to boat strike. Cases were diagnosed with trauma
or lacerations of unknown cause when clear evidence
for shark attack or boat strike was not
detected.
Causes of death were rigorously standardized
so that the primary cause identified for each
otter was the most substantial injury or illness
initiating the sequence of events leading directly
to death. Otters were assigned two equally
weighted primary causes of death if two unrelated
and independent conditions were each
severe enough to have caused death. Contributing
causes of death were noted only if pathologic
conditions were identified that added to
the probability of death, but were not part of
the primary disease complex. To ensure independence
of primary and contributing causes
of death, diagnoses of conditions were based
solely on the severity of the individual lesions
regardless of other conditions present.
Statistical analyses
Proportionate mortality, noted as a percent,
was used to identify the major causes of death
in sea otters from 1998 to 2001. Cause-specific
proportionate mortality was calculated as the
proportion of otters with a specific condition as
the primary cause of death among all otters
that met the inclusion criteria during the study
period. Distribution of the four most common
causes of death among sex and age classes was
evaluated by the standard two-sided chi square
test of independence using statistical software
(Epi Info Version 6, Centers for Disease Control
and Prevention, Atlanta, Georgia, USA).
One-sided chi-square test of independence was
used to test associations between each of the
four most common primary causes of death and
the common contributing causes of death with
at least nine cases each. If age or sex were significantly
associated with a primary cause of
death, associations among primary and contributing
causes of death were stratified by the significant
variable (age or sex), and the association
was evaluated for each stratum. For dichotomous
distributions with an expected frequency
less than five, the Fisher exact test
(Fisher, 1935) was calculated using statistical
software (SPSS Base 10.0, SPSS Inc., Chicago,
Illinois, USA). When appropriate, strength of
the association was estimated by the odds ratio.
Geographic and temporal clustering of overall
carcass retrieval and temporal clustering of
each primary cause of death were evaluated by
the scan test (Carpenter, 2001). This test evaluates
whether carcass retrieval was uniform using
the binomial distribution to estimate the
probability of the maximum observed number
of cases within sequential distances of 5 km, 10
km, 15 km, and 20 km for geographic clustering
and within 1, 2, 3 and 4 mo for temporal
clustering. These spatial and temporal periods
were specified because increased carcass retrieval
within these time periods was considered
biologically significant based on sea otter
behavior and habitat use. Geographic clustering
of specific primary causes of death was evaluated
only for the four most common primary
causes of death with 10 cases or more. Specifically,
the spatial scan statistic (Kulldorf and
Nagarwalla, 1995) was used to test whether a
primary cause of death was randomly distributed
along the coastline where sea otters carcasses
were recovered. The Bernoulli model
was selected for this procedure, which used the
case and control approach to adjust for differential retrieval of carcasses along the coastline.
In this manner, stranding locations for each
specific cause of death were compared to locations
for otters with all other causes of death.
A Monte Carlo iterative technique was used to
determine distribution of the likelihood ratio
test statistic (Kulldorf and Nagarwalla, 1995).
 
RESULTS

Between February 1998 and June 2001,
105 sea otter carcasses met our inclusion
criteria and received a complete necropsy
and diagnostic work up in order to determine
the cause of death. Of these otters,
27 were alive at the time of stranding but
died or were euthanized at rehabilitation
centers. Sea otter carcass retrieval was spatially
clustered along the coastline during
our study period. Both Monterey Bay and
Estero Bay had significant (P,0.01) clusters
of beachcast carcasses. No carcasses
were retrieved from the remote and rocky
140 km long coastal segment in the center
of the sea otter range south of Yankee
Point (368489N, 1218949W) to north of San
Simeon Point (358639N, 1218199W). Overall
carcass retrieval was not temporally
clustered during the study period. Carcasses
recovered consisted predominantly
of prime-aged adults (46.7%), with fewer
juveniles (29.5%), subadults (11.4%), and
aged adults (12.4%). Distribution of primary
causes of death among sex and age
classes is shown in Table 1. While 25 different
primary causes of death were identified,
53.3% of otters (56/105) died from
one of four major causes: T. gondii encephalitis,
acanthocephalan parasite infection,
shark attack, or cardiac disease. Acanthocephalan
infection, cardiac disease, and
T. gondii encephalitis were also recognized
as common contributing causes of death
(Table 1).
Encephalitis due to T. gondii was one of
the two leading causes of mortality identified
in sea otters during the time period
studied. This condition, characterized by
moderate to severe, multifocal, non-suppurative
and necrotizing meningoencephalitis
(Fig. 1), was a primary cause of death
in 16.2% of the otters examined and was
a contributing factor in another 11.4% of
otters examined. A marginally significant
spatial cluster of T. gondii encephalitis cases
was detected in a 25 km area at the
southern end of Estero Bay in central California
(P50.06, centered at 358319N,
1208889W, Fig. 3). Half of the otters (8/16)
recovered in this section of Estero Bay
were determined to have T. gondii encephalitis
as the primary cause of death.
Encephalitis caused by S. neurona was
characterized by severe, necrotizing,
mixed non-suppurative and suppurative
encephalitis, which was often most severe
in the cerebellum and brainstem. Encephalitis
due to S. neurona was the primary
cause of death identified in 6.7% of otters,
all of which were detected during spring
months (March through May). Cases were
significantly clustered temporally in the
spring of 2001 (P50.01). Purely suppurative
encephalitis was detected in only one
sea otter, but the primary cause of death
in this case was attributed to facial bite
wounds, which caused a ganglioneuritis
and ascending infection with Archanobacterium
phocae. Encephalitis of unknown
or unconfirmed cause was a primary cause
of death for another 4.8% of otters examined.
Overall, encephalitis of all types
caused death in 28% of otters examined
and contributed to death in another 18%
of otters.
Similar in proportionate mortality to T.
gondii encephalitis, infection with acanthocephalan
parasites was a primary cause
of death in 16.2% of otters examined, and
this parasite contributed to death in another
9.5% of otters. Septic peritonitis, caused
by migrating Profilicollis spp., was the
most common consequence of heavy acanthocephalan
infection (Fig. 4). This type of
peritonitis was the primary cause of death
in 14.3% (15/105) of otters examined and
was 3.5 times more likely to have caused
death in juveniles and subadults than
adults or aged adults (two-sided chi square
test, P50.03). Acanthocephalan infection
either directly caused, or was a contributing
factor for, death in 40% (17/43) of the juvenile and subadult otters examined. A
geographic cluster of acanthocephalan
peritonitis was detected at the southern
end of Monterey Bay (P50.02, centered at
368609N, 1218889W, Fig. 3). In this 1.8 km
area, five of six carcasses recovered had
acanthocephalan peritonitis as a primary
cause of death, while only one case was
expected if this condition had been distributed
evenly across locations where carcasses
were recovered along the coast. The
sixth carcass recovered in this area had
acanthocephalan peritonitis as a contributing
cause of death.
Shark-inflicted mortality was detected in
13.3% of otters examined. All cases had
bite wounds that were consistent with attack
by white sharks (Carcharodon carcharias,
Fig. 2). A significant spatial cluster
of otters attacked by sharks was noted in
the 80 km stretch of coastline from Point
An˜ o Nuevo to Santa Cruz (P50.02, centered
at 378119N, 1228339W, Fig. 3). In this
area, six of 10 otters recovered were killed
by sharks, while only 1.3 cases of shark attack
were expected had this condition
been distributed evenly in areas where
carcasses were recovered. Histopathologic examination of brain tissue from shark-attacked
otters revealed that eight of 14 otters
(57%) attacked by sharks had pre-existing
encephalitis. Otters with moderate
to severe T. gondii encephalitis were 3.7
times more likely to be attacked by sharks
than otters without this condition (one-sided
Fisher exact test, P50.05). Shark-inflicted
mortality was not significantly associated
with acanthocephalan infection,
cardiac disease, or emaciation.
Cardiac lesions in otters were newly recognized
during this study period and cardiac
disease was diagnosed as a primary
cause of death in 13.3% of otters examined.
Cardiac lesions consisting of mild to
severe non-suppurative (lymphocytic)
myocarditis (Fig. 5) were a common finding
in otters examined (n541). These lesions
were considered a cause of death
only when myocarditis was accompanied
by a grossly enlarged, rounded, dilated,
and thin walled heart (Fig. 5) and/or
strong evidence for congestive heart failure
(pulmonary edema, pleural and peritoneal
effusion, and hepatic congestion).
Nearly all cardiac disease cases were observed
in prime-aged adults or aged adults,
and this condition was 3.5 times more likely
to be a primary cause of death in females
than males (two-sided chi square
test, P50.04). Severe nose wounds were found in half of the otters (7/14) with cardiac
disease as a primary cause of death.
Nose wounds are commonly acquired by
females during mating (Staedler and Riedman,
1993) but also result from intraspecific
aggression in males. Both male otters
with severe nose wounds had cardiac disease
as a primary cause of death (one-sided
Fisher exact test, stratified on sex,
P,0.01) and five of nine female otters with
severe nose wounds had cardiac disease as
a primary cause of death (one-sided Fisher
exact test, stratified on sex, P50.01). In all
cases, severe nose wounds were acute or
subacute and seemed to have occurred after
development of cardiac disease. While
significant localized geographic clusters of
cardiac disease cases were not detected,
otters with this condition were 5.6 times
more likely to be recovered from the
southern half of the California sea otter
range (two-sided chi square test, P,0.01),
which is also where the cluster of T. gondii
encephalitis was detected. Otters diagnosed
with cardiac disease were 2.9 times
more likely to have concurrent T. gondii
encephalitis than otters without cardiac
disease (one-sided chi square test,
P50.01). Cardiac disease was not associated
with any other common contributing
cause of death.
While emaciation was not determined
to be a primary cause of death in any otters
examined, emaciation was identified
as a contributing cause of death in 15% of
otters. Emaciation was most significantly
associated with cardiac disease (one-sided
Fisher exact test, P50.01) and was 3.2 times more likely to be a contributing
cause of death in females than males (twosided
chi square test, P50.03). Of 27 adult
and aged adult females that were necropsied,
nine were confirmed to be lactating
at the time of death. Most lactating females
(7/9) were emaciated at death and
four of nine lactating females had cardiac
disease as a primary cause of death.
Infectious diseases (caused by parasites,
bacteria, and fungi) and diseases without a
specified etiology (cardiac disease, intestinal
disease, and encephalitis of unconfirmed
cause) were implicated as a primary
cause of death in 63.8% of otters examined.
Disease was most commonly a primary
cause of death in prime-aged adults
(n530) compared to juveniles (n519),
subadults (n510), and aged adults (n58).
Parasitic diseases alone, caused by T. gondii,
S. neurona, and Profilicollis spp, were
determined to be a primary cause of death
in 38.1% of the otters examined.

DISCUSSION

Encephalitis, caused by T. gondii and S.
neurona, was first recognized as a source
of mortality in sea otters only after detailed
necropsies were begun in 1992 (Cole et
al., 2000; Lindsay et al., 2000; Miller et al.,
2001a). Because encephalitis can only be
diagnosed by microscopic examination of
brain tissue, this cause of death was likely
missed in the past when carcasses were
not examined in such detail. However, the
reported percent of mortality attributed to
protozoal encephalitis appears to have increased
substantially over the short period
during which detailed examinations have
been undertaken. Of otters examined from
1992–95, 8.5% had protozoal encephalitis
while 22.9% of otters we examined had
protozoal encephalitis as a primary cause
of death. This apparent increase in prevalence
may be a consequence of improved
diagnostics, a difference in criteria for establishing
this diagnosis among laboratories
and pathologists, or temporal variation
in the occurrence of this disease. Other
causes of encephalitis should also be considered,
particularly for cases with an as
yet unconfirmed cause. However, the magnitude
of this most recent temporal trend
certainly warrants attention, particularly as
the increased prevalence of this condition
coincides with a period of population decline.
Protozoal infections in sea otters may be
examples of spillover of land-based pathogens
into the marine ecosystem because
the only identified definitive hosts for T.
gondii and S. neurona are felids and opossums
(Didelphis virginiana), respectively.
The spatial cluster of mortality due to T.
gondii encephalitis in Estero Bay may be
a consequence of local factors, such as increased
sea otter exposure to T. gondii, enhanced
parasite virulence, or increased sea
otter susceptibility in this particular area.
In a separate study, sea otter carcasses
found in Estero Bay had higher prevalence
of antibodies to T. gondii than otters sampled
elsewhere (Miller et al., 2002), suggesting
that mortality may be due to high
levels of parasite exposure. Seasonal peaks
of T. gondii encephalitis mortality in otters
were not detected even though coastal
freshwater runoff has been associated with
increased odds of exposure to T. gondii in
sea otters (Miller et al., 2002). Runoff is
highest during the winter rainy season and
spring in California. However, many unrecognized
environmental and host factors
could affect the timing of death from this
disease. Otters with S. neurona encephalitis,
which may be a more acutely severe
and rapidly progressive disease, stranded
only in spring months (March through
May), which follows maximal seasonal runoff
and coincides with the season when
opossums were more likely to shed sporocysts
(Rickard et al., 2001).
While infection with T. gondii is common
in terrestrial mammals, it is usually
subclinical in immune competent hosts
(Frenkel, 1988). Disseminated systemic
disease with severe brain infection is more
typical of immune suppressed humans,
such as HIV infected AIDS patients (Arnold
et al., 1997). Fatal T. gondii infections have been reported in neotropical marsupials
and nonhuman primates, which
evolved in ecologic isolation from domestic
cats (Frenkel, 1988). Expansion of domestic
cat and opossum populations and
decreased natural filtration of watershed
runoff through coastal estuaries may have
increased sea otter exposure to a pathogen
for which they are immunologically ill-prepared.
These protozoal pathogens are not
likely to have been abundant in the marine
environment centuries ago. The substantial
proportionate mortality caused by protozoal
encephalitis in juvenile and prime
aged adult otters is of concern, particularly
because T. gondii encephalitis was shown
here to be associated with two other important
causes of death, shark attack and
cardiac disease. If T. gondii infection increases
the risk of death from shark attack
or cardiac disease, this parasite may have
a complex but critical role in a high level
of mortality in sea otters.
Toxoplasma gondii infection may have
other deleterious effects that are difficult
to document by the methods used here.
Fetal infection with T. gondii is associated
with serious birth defects and a high frequency
of abortion in terrestrial animals
and humans. These effects would be difficult
to detect in free-living sea otters because
aborted fetuses and pups that die
shortly after birth are less likely to be
found in fresh condition. Underlying causes
for the perinatal mortality noted in recovered
pup carcasses could not be determined
but all were near full term pups
that died shortly after birth and none had
pathologic findings consistent with protozoal
infection.
The high prevalence of pre-existing T.
gondii encephalitis in shark attacked otters
suggests that otters with encephalitis may
exhibit aberrant behavior that renders
them more vulnerable to attack by sharks.
Otters with protozoal encephalitis frequently
exhibit fine muscle tremors, recurrent
seizures, dull mentation, and decreased
or abnormal motor function (M.
Murray, pers. comm.). Neurologic dysfunction
might cause otters to be less able
to evade attacks, to move offshore out of
the protected areas, or to attract shark attention
through abnormal movements and
seizures. Wounds inflicted upon otters by
sharks were typically large gashes with
minimal soft tissue removal, consistent
with open-mouth slashing or raking by
sharks (Fig. 2). This bite pattern is similar
to that seen when sharks attack humans
(Byard et al., 2000) and is not consistent
with a bite pattern used for intended prey.
Sharks feeding on pinniped prey often remove
large pieces of soft tissue (Lucas and
Stobo, 2000). The wound pattern observed
in otters suggests that they may not be intended
prey and the high percent of sharkattacked
otters with pre-existing encephalitis
is consistent with the hypothesis that
sharks are more likely to attack otters if
they are acting abnormally.
The area from Santa Cruz to Point An˜ o
Nuevo with high shark-related mortality in
sea otters is known for white shark predation
on pinnipeds (Long et al., 1996).
Shark-inflicted mortality has been longrecognized
as an important cause of mortality
in sea otters since carcasses were first
evaluated in 1968 and the number of
shark-bitten beachcast carcasses has varied
considerably by year (Ames et al., 1996).
However, the annual proportion of sharkattacked
sea otter carcasses relative to the
annual population count has increased
through time particularly during periods of
population decline (Estes et al., 2003). Because
interactions with sharks may be
modified by encephalitis in otters, prevalence
of shark attack may be linked to
prevalence of encephalitis. Both shark attack
and encephalitis may be under-represented
as a cause of death if carcasses
with penetrating wounds from shark bites
are more likely to sink than wash ashore
(Lucas and Stobo, 2000) or if otters are
consumed by sharks, although the latter
has never been observed.
Cardiac disease has not previously been
reported in sea otters and the substantial
percent of deaths attributed to cardiac disease was unexpected. Stress-related cardiac
disease has been documented in
stranded cetaceans (Turnbull and Cowan,
1998), but the contraction band-necrosis
of myocardium detected in dolphins and
whales differed from the pattern of nonsuppurative
myocarditis and gross cardiac
dilation observed in sea otters. The inflammatory
nature of the cardiac lesions noted
here suggests an infectious etiology although
infectious agents were not detected
during microscopic examination of sea
otter myocardium. Our observation that
otters with cardiac disease are more likely
to have concurrent T. gondii encephalitis
implies that these two conditions are causally
linked or are somehow coupled by an
unknown mechanism. Rare accounts of
myocarditis in animals infected with T.
gondii have been reported in dolphins
(Inskeep et al., 1990), a northern fur seal
(Callorhinus ursinus; Holshuh et al.,
1985), and a California sea lion (Zalophus
californianus; Migaki et al., 1977), although
disseminated toxoplasmosis with
protozoal cysts in cardiac myofibers were
observed in all cases. In humans, T. gondiirelated
cardiomyopathy has been documented
in AIDS patients (Matturri et al.,
1990) and immune-suppressed heart
transplant patients (Arnold et al., 1997).
Efforts are currently being directed at understanding
the immunopathology of toxoplasmosis
in sea otters, improving detection
methods for protozoal stages, and
evaluating other possible etiologies and
risk factors for cardiac disease.
Cardiac disease was a common cause of
death in female otters and was often associated
with severe nose wounds and
emaciation. Emaciation and severe nose
wounds may be a secondary consequence
of the debilitating effects of heart failure,
which could prevent afflicted otters from
foraging effectively and defending themselves
against aggressive males. Adult females
appear to be highly susceptible to
both mating trauma and emaciation, particularly
at the end of lactation, possibly
because they are at a nutritional disadvantage
after caring for a pup and entering
estrus, which attracts male attention. The
transition from pup care and lactation to
estrus and breeding appears to be a particularly
vulnerable period for adult female
sea otters in California.
Acanthocephalan peritonitis continues
to be a substantial cause of mortality in sea
otters, and the recent prevalence (16.2%)
is similar to the 14% reported from 1992–
95 (Thomas and Cole, 1996). Sand crabs
(Emerita analoga) and possibly spiny mole
crabs (Blepharipoda occidentalis) serve as
intermediate hosts for these acanthocephalan
parasites (Hennessy and Morejohn,
1977), and these crabs are found in predominantly
sandy habitat. It is therefore
likely that otters foraging in sandy bays will
have a high level of exposure to Profilicollis
spp. As expected, mortality due to acanthocephalan
peritonitis during this study
period was detected exclusively in carcasses
retrieved from Monterey Bay and Estero
Bay, both of which are largely sandy
habitat. While sand crabs may not be preferred
sea otter prey, they are abundant
and easy to capture. Juvenile otters may
ingest large numbers of these prey species
when they are first searching for suitable
home-range habitat and learning to forage
on their own, which may explain the high
level of exposure and subsequent mortality
in this age class.
Even though acanthocephalan peritonitis
is readily apparent at necropsy through
gross evidence of peritonitis associated
with parasites in the abdominal cavity, this
condition was reported only once in necropsies
performed on otters from 1968–76
(Hennessy and Morejohn, 1977), suggesting
that fatal acanthocephalan infections
may have increased in prevalence. The apparent
increased prevalence of acanthocephalan
peritonitis may reflect increased
host susceptibility to infection or increased
exposure through a shift in preferred prey
availability, intermediate host abundance,
foraging behavior, or habitat use. Southerly
otter range expansion into the predominantly
sandy habitat south of Point Estero is unlikely to have contributed substantially
to the higher prevalence of this
condition in recent years because 80% of
the otters with fatal acanthocephalan infections
from 1998–2001 were retrieved
from Monterey Bay, which has been occupied
by sea otters since the 1970s (Riedman
and Estes, 1990).
Domoic acid intoxication has not been
previously reported in sea otters and necropsy
findings and preliminary laboratory
tests suggest that domoic acid intoxication
was a primary cause of death in four otters
examined here. Domoic acid is a marine
biotoxin produced by Pseudonitzchia spp.
and is known to cause severe neurologic
dysfunction and death in California sea lions
(Scholin et al., 2000) and seabirds
(Work, 1993). Domoic acid exposure
caused characteristic brain and cardiac lesions
in sea lions (Scholin et al., 2000), and
histologic lesions associated with domoic
acid exposure in sea otters are currently
being evaluated. Domoic acid intoxication
may be established as a more common
cause of mortality in sea otters once diagnostic
capabilities are refined and
screening is performed more routinely.
Coccidioidomycosis, caused by the soil
fungus C. immitis was diagnosed as a primary
cause of death in only one otter (1%)
during our study period. In otters examined
from 1992–95, eight cases had severe
disseminated coccidioidomycosis (Thomas
and Cole, 1996), so there may be some
variation in mortality due to this pathogen.
Our approach of identifying more than
one primary cause of death in sea otters
with two equally severe, yet independent,
causes of death has resulted in slightly
higher proportionate mortality for some
conditions than if diagnoses had been limited
to one primary cause of death per otter.
This strategy allowed for an unbiased
account of important causes of death, but
the proportionate mortality reported here
may not be comparable to mortality studies
using more traditional methods. Also,
many of these causes of mortality may be
subject to substantial inter-annual variation
and other causes of mortality are likely
to be identified retrospectively as new
diagnostic techniques are developed and
implemented as screening tools.
In this study, carcasses were recovered
primarily along accessible sandy shores.
Sea otter carcasses are not likely to wash
ashore along rocky precipitous coastlines
and those that do are not likely to be recovered
while in fresh condition because
most of these areas are not readily accessible. 
[3] Therefore, very little is known of
causes of mortality in sea otters living
along the rocky and remote coastline in
the center of the sea otter range in California.

A directed search effort would be
necessary to collect fresh carcasses from
these unpopulated and inaccessible areas.
An estimated one-half of all recently deceased
sea otters were recovered as beachcast
carcasses, and one-fourth of these
were retrieved in adequately fresh condition
to allow detailed necropsy for specific
cause of death determination (Estes et al.,
2003). Based on these estimates and the
specific inclusion criteria for this study, approximately
one of ten deceased southern
sea otters was evaluated. Because the age
distribution of carcasses reported here
closely matches the age distribution of all
carcasses recovered recently (Estes et al.,
2003), the carcasses included in this study
are likely to be representative of all recovered
carcasses. Consequently, the major
causes of death reported here are probably
similar to what would be observed if detailed
cause of death information could be
obtained from decomposed or heavily
scavenged carcasses. While a relatively
high proportion of the population was
available for cause of death determination,
certain causes of death, such as drowning
due to accidental entanglement in fish
traps or nets, may be under-represented in
beachcast carcasses. These carcasses may
be less likely to float and wash ashore prior
to decomposing, and drowning is very difficult
to document even with detailed necropsy.
Therefore, the cause-specific proportionate
mortality reported here may not be directly referable to the southern
sea otter population.
Identification of pathogens responsible
for substantial morbidity and mortality in
sea otters and the geographic distribution
of these pathogens is an important first
step toward understanding the role of population
health in the recovery of this
threatened species. However to fully understand
the underlying mechanisms creating
the observed pattern of mortality,
factors that may be affecting nutrition, immune
system competency, and sources of
increased pathogen exposure must be evaluated.
Studies have detected elevated tissue
levels of potentially immunotoxic contaminants
in southern sea otters with infectious
disease (Kannan et al., 1998; Nakata
et al., 1998), but immune system
function in wild animals is difficult to measure
because species-specific tests must be
developed and validated for different age
classes.
The high percent of prime-aged adults
among beachcast sea otter carcasses in
California, and the very high prevalence of
disease noted in this age class are not consistent
with a healthy population destined
for recovery. Sea otter populations experiencing
a decline from increased levels of
mortality typically have a high percent of
prime-aged adults among beachcast carcasses
(Estes et al., 2003). Certainly, the
prevalence of acanthocephalan-related disease
in juveniles and the prevalence of T.
gondii encephalitis, cardiac disease, and
shark attack in prime aged adults have the
potential to exert a population-level effect
and may be limiting sea otter population
growth in California. The underlying processes
promoting increased levels of parasitic
disease in sea otters should be a focus
of future investigation. Special attention
should be given to non-native terrestrial
species that are endemically infected
with protozoal pathogens and have the capacity
to serve as a reservoir for persistent
exposure and infection in sea otters. Recovery
of the southern sea otter population
may face a significant challenge as this isolated
population struggles to expand in a
near-shore system that may have been substantially
altered in terms of prey abundance,
water quality, and pathogens in the
time since the near-extirpation and early
recovery of sea otters.
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