Page 1
MAJOR PATHOLOGIC FINDINGS AND PROBABLE CAUSES OF
MORTALITY IN BOTTLENOSE DOLPHINS STRANDED IN SOUTH
CAROLINA FROM 1993 TO 2006
Wayne E. McFee,1,3 and Thomas P. Lipscomb2
1 National Oceanic and Atmospheric Administration, National Ocean Service, Center for Coastal Environmental Health
and Biomolecular Research, 219 Fort Johnson Road, Charleston, South Carolina 29412, USA
2 Armed Forces Institute of Pathology, Department of Veterinary Pathology, Washington, D.C. 20306, USA
3 Corresponding author (email: wayne.mcfee@noaa.gov)
ABSTRACT: Although cause-of-death information on bottlenose dolphins (Tursiops truncatus) can
be located in the literature, few citations include mortality data over a long period of time covering
a broad geographic region. This study describes major pathologic findings and probable causes of
death of bottlenose dolphins over a 14-yr period (1993–2006) for the coastal region of South
Carolina. Probable causes of death for 97 cases were determined based on gross pathology and
histopathology. In an additional 30 cases, probable cause of death was apparent from gross
pathology alone, and carcass condition precluded histopathology. Of the 97 dolphins examined
grossly and histologically, 30 (31%) likely died of infectious disease and 46 (47%) of noninfectious
disease; the cause of death was unknown in 21 (22%). Bacterial infections accounted for the large
majority of fatal infections and emaciation was the leading cause of noninfectious mortality. Twelve
dolphins were killed by human interactions. Of the 30 dolphins diagnosed from gross examination
alone, 23 likely died from human interaction and seven were killed by stingray-spine inflictions.
Although the absence of consistent use of microbiology, biotoxin analysis and contaminant testing
decreases the conclusiveness of the findings, this study has broad implications in establishing
baseline data on causes of death of bottlenose dolphins for future studies and for the detection of
emerging diseases.
Key words: Bottlenose dolphin, cause of death, mortality, South Carolina, strandings,
Tursiops truncatus.
INTRODUCTION
Information on the causes of mortality
of bottlenose dolphins (Tursiops trunca-
tus) over many years for a broad geo-
graphic region has been sparse. Most of
the information in the literature on this
topic is limited to mortality of bottlenose
dolphins that involve periods of increased
mortality or descriptions of pathologic
findings in small numbers of individuals
(Lipscomb et al., 1994; Krafft et al., 1995;
Lipscomb et al., 1996; Bossart et al., 2003;
McFee and Osborne, 2004).
Bottlenose dolphins can be regarded as
sentinel species of the oceans, providing
an indication of disease processes and
environmental problems (Bossart, 2006)
that could affect marine animal and
human health. Several studies have de-
scribed the presence of high levels of
contaminants in bottlenose dolphins as a
potential cause of reproductive stress and
debilitative disease (Schwacke et al., 2002;
Hansen et al., 2004; Houde et al., 2005;
Wells et al., 2005). Because humans and
dolphins compete for many of the same
food resources (i.e., fish, shrimp, and
squid) and reside in close proximity,
knowledge regarding dolphin disease
could act as an indicator of emerging
diseases about which humans may need to
be concerned. Likewise, interactions of
dolphins with fishery operations have
been demonstrated to impact both the
health and well being of dolphins and the
economics associated with fisheries nega-
tively (International Whaling Commission
[IWC], 1994).
Concern over bioterrorism has prompt-
ed a change in perspective on biologic and
environmental data. In their role of
sentinels of the oceans, dolphin strandings
and causes of death could aid in the
detection of biologic or chemical agents
that may be harmful to human health.
Federal and state agencies in South
Journal of Wildlife Diseases, 45(3), 2009, pp. 575–593
# Wildlife Disease Association 2009
575
Page 2
Carolina are developing an Environmental
Surveillance Network (ESN), the partici-
pants of which will share biologic (e.g.,
marine mammal mortalities, fish kills,
harmful algal blooms) and environmental
data (e.g., water quality, chemical spills) to
detect environmental risks in near real
time (University of South Carolina–Center
for Public Health Preparedness [USC-
CPHP], 2007). This integration of data at
the state level could be directed to
national emergency response systems such
as the Biological Warning and Incident
Characterization System (BWIC) estab-
lished by the Department of Homeland
Security (Sandia National Laboratories,
2006).
The South Carolina coastline consists of
numerous estuaries and barrier islands in
the lower three-quarters of the state
(approximately 301 km) south of Murrells
Inlet (33.5312uN and 279.0312uW). The
northern quarter of the state (approxi-
mately 101 km), commonly known as the
Grand Strand, is generally a continuous,
gently sloping beach. Resident popula-
tions of dolphins have been described in
the estuaries in and around Hilton Head
Island (Petricig, 1995) and Charleston,
South Carolina, USA (Zolman, 2002).
However, stock structure of Western
North Atlantic (WNA) coastal bottlenose
dolphins is believed to be more complex
than was previously described (Scott et al.,
1988; Hohn, 1997; McLellan et al., 2002).
Presently, the National Marine Fisheries
Service recognizes seven stocks of WNA
bottlenose dolphins ranging from New
Jersey to Florida (Waring et al., 2006).
These Management Units (MU) are based
on genetic analysis, photoidentification
studies, and shipboard and aerial surveys.
Bottlenose dolphins in South Carolina are
believed to be from two of these MUs: the
Southern North Carolina MU (SNCMU)
and the South Carolina MU (SCMU;
McFee et al., 2006). The SNCMU extends
from Cape Lookout, North Carolina to
Murrells Inlet, South Carolina. Dolphins
in South Carolina that are in the SNCMU
are believed to be migratory in nature
based on seasonal stranding trends
(McFee et al., 2006) and the presumption
that no resident estuarine population of
bottlenose dolphins has been observed
north of North Inlet (33.3258uN and
279.1608uW; Young and Phillips, 2002)
in South Carolina. The SCMU extends
from Murrells Inlet to the Savannah River
(32.0391uN and 20.8853uW) bordering
Georgia. As such, migratory dolphins that
spend most of their lives along the coast
and resident, estuarine dolphins that are
exposed to increased pressure from an-
thropogenic activities have the potential to
vary in their disease processes and level of
anthropogenic impact.
The main objective of this study was to
determine probable causes of death of
bottlenose dolphins based on necropsies
over a 14-yr period (1993–2006) for the
coastal region of South Carolina. In
particular, spatial trends were analyzed,
as well as age-specific causes of mortality.
MATERIALS AND METHODS
Carcasses of bottlenose dolphins stranded in
South Carolina were examined and necropsied
according to standard procedures (Geraci and
Lounsbury, 1993; McFee et al., 2006). In most
cases, carcasses were transported to the
National Ocean Service’s (NOS) Center for
Coastal Environmental Health and Biomolec-
ular Research (CCEHBR) in Charleston,
South Carolina, USA. Carcasses that could
not be transported to CCEHBR were necrop-
sied on site or moved to a suitable location for
necropsy. In general, only tissues from fresh
dead (code 2) animals were examined histo-
logically. On occasion, tissues from moderately
decomposed (code 3) animals were analyzed
histologically if unusual lesions were observed
or to investigate further evidence of death
caused by interactions with humans (e.g.,
fishery entanglement).
Tissues of all the major organs and lesions
were collected and stored in a fixative solution
of 10% neutral buffered formalin (NBF).
From 1993 to 2003, the formalin-fixed tissues
were subsampled into approximately 1-cm
cubes, wrapped in formalin-soaked gauze,
placed in individual Ziploc bags, and shipped
overnight to the Armed Forces Institute of
Pathology (AFIP), Department of Veterinary
576 JOURNAL OF WILDLIFE DISEASES, VOL. 45, NO. 3, JULY 2009
Page 3
Pathology (Washington, D.C., USA) for histo-
logic analysis. Beginning in 2004, collected
tissue samples were placed directly into
Omnisette tissue cassettes (Fisherbrand),
soaked in 10% NBF for at least 24 hr, and
then shipped overnight to the AFIP. Sections
of the following tissues were collected from
most dolphins: lung, muscle, liver, kidney,
heart muscle (all four chambers), aorta,
pericardium, pancreas, spleen, major bronchi,
stomach chamber lining, esophagus, dia-
phragm, thymus, thyroid gland, cerebellum,
cerebrum, brain stem, lung-associated lymph
nodes, mesenteric lymph nodes, prescapular
lymph node, pulmonary lymph node, sternal
lymph node, intestine, tongue, adrenal glands,
rectal gland, colon, and reproductive organs.
Formalin-fixed tissues were embedded in
paraffin, sectioned at 5 mm, and stained with
hematoxylin and eosin for examination by light
microscopy. Selected sections were stained
with Brown and Hopps Gram’s stain, Brown
and Brenn Gram’s stain or by Grocott’s
methenamine silver nitrate method.
Age was determined from thin sections of
postnatal dentine observed in the teeth
following Hohn et al. (1989). Age classes were
separated into neonate (#0.1 yr), calf (.0.1–
1 yr), juvenile (.1–9 yr), and adult (.9 yr). In
cases where a tooth was not available for aging,
dolphins were placed in one of the four
categories based on their length
(,120 cm5neonate; 121–1505calf; 151–
230 cm5juvenile; .230 cm5adult).
In formulating our assessment of the cause
of death, we used the following definition:
‘‘Cause of death—the disease, injury, or
abnormality that alone or in combination is
responsible for initiating the sequence of
functional disturbances, whether brief or
prolonged, that eventually ends in death’’
(Froede, 1990). After determining the proba-
ble cause of death, the death was categorized
as infectious or noninfectious. The infectious
and noninfectious diseases were further de-
fined based on the specifics of the cases.
There were a number of dolphins judged to
have died as a direct result of human
interaction from which tissues were not
collected for histology because of postmortem
decomposition or artifacts caused by freezing
of the carcass. The diagnosis of death likely
due to human interaction by entanglement in
fishing gear was based on combinations of the
following criteria: fishing gear attached to the
body, evidence of net or rope wounds,
persistent froth in airways, edematous lungs,
evidence of recent feeding, good nutritional
condition, and exclusion of other causes of
death (Kuiken, 1996). The diagnosis of death
likely due to boat collision was based on
combinations of the following criteria: evi-
dence of boat propeller wounds, fractures,
contusions, exclusion of other causes of death
and (in one case) eyewitness observation of the
incident.
Locations of bottlenose dolphins analyzed in
this study were plotted on a map with the use
of ArcMap 9.1 (Environmental Systems Re-
search Institute [ESRI], 2005). For pathologic
differences, dolphins were separated into
those that were examined or stranded from
two geographic locations, the southern portion
of the SNCMU (Little River, South Carolina
[33.8686uN and 278.4997uW] to Murrells
Inlet) and the SCMU (Murrells Inlet to
Savannah River; Fig. 1).
RESULTS
During the period 1993 to 2006, 550
bottlenose dolphins were reported floating
dead, stranded dead on beaches or in
estuaries, alive and stranded, or alive and
entangled. Of these, 453 were inaccessible
or in an advanced stage of decomposition
and not suitable for histologic examination
when reached. Complete or partial nec-
ropsies were performed on 302 carcasses.
Tissues were sufficiently well preserved
for histologic examination in 97 (42 male
[M]:55 female [F]) cases (17.6% of the
total reported strandings). Data on these
dolphins, including significant pathologic
findings, likely cause of death, and cause
of death category, are summarized in
Table 1. Additionally, likely cause of death
could be reasonably assessed by gross
examination alone in an additional 30
cases. Similar information from these
dolphins is presented in Table 2. Cause-
of-death information on all 127 dolphins is
summarized in Table 3.
Ages were determined based on tooth
examination for 98 (77.2%) dolphins. The
remaining 29 dolphins were placed into
age classes based on their lengths. Nine-
teen dolphins comprised the neonate class
(9 M/10 F), 14 dolphins comprised the calf
class (6 M/8 F), 42 comprised the juvenile
class (23 M/17 F/2 unknown [U]), and 51
comprised the adult class (16 M/33 F/2
U). One animal (case 112) of unknown sex
MCFEE AND LIPSCOMB—PATHOLOGIC FINDINGS IN BOTTLENOSE DOLPHINS 577
Page 4
and age class was released dead from a
crab-pot buoy line but was not necropsied.
Of the 97 dolphins examined grossly
and histologically, 30 (31%) likely died of
infectious disease and 46 (47%) of nonin-
fectious disease; the cause of death was
unknown in 21 (22%). Thus, of the 76
dolphins examined grossly and histologi-
cally for which the likely cause of death
was determined, 30 (39.5%) died of
infectious diseases, and 46 (60.5%) died
of noninfectious diseases. The number of
dolphins in each age class and in each
cause of death category is summarized in
Table 4.
DISCUSSION
Bacterial infections comprised the larg-
est group of fatal infections (21 cases) and
most of these were septicemias and/or
bacterial pneumonias. These diagnoses
were based on histopathology; bacterial
cultures were not routinely performed.
Bacterial pneumonia has been found to be
common in other studies of dolphin
mortality (Howard et al., 1983; Baker,
1992). More recent studies suggest that
some bacterial infections in dolphins may
have their source from sewage outfalls,
though this still remains speculative (Par-
sons and Jefferson, 2000; Greig et al.,
2007). There were five cases of verminous
pneumonia and one case of pneumonia
that was primarily verminous with a lesser
component of fungal hyphae. The identity
of the fungus was not determined. The
lungworms were compatible with Halo-
cercus lagenorhynchi based on histomor-
phology. Lungworm infection is very
common in bottlenose dolphins and is
generally considered to be of little clinical
significance, but the severe pneumonias in
these cases appeared to be the causes of
death. Evidence of prenatal infection of
bottlenose dolphins by these parasites has
FIGURE 1. Stranding locations of bottlenose dolphins in South Carolina analyzed in the three cause-of-
death categories.
578 JOURNAL OF WILDLIFE DISEASES, VOL. 45, NO. 3, JULY 2009
Page 5
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p
n
eu
m
o
n
ia
an
d
ly
m
p
h
ad
en
it
is
;
ab
sc
es
se
s
in
d
ia
p
h
ra
gm
,
b
lu
b
b
er
,
sk
in
,
sk
el
et
al
m
u
sc
le
;
em
ac
ia
ti
o
n
D
is
se
m
in
at
ed
b
ac
te
ri
al
in
fe
ct
io
n
/s
ep
ti
ce
m
ia
In
fe
ct
io
u
s
d
is
ea
se
(b
ac
te
ri
al
)
1
6
2
6
1
0
8
2
3
1
3
N
o
ve
m
b
er
1
9
9
7
A
F
B
ac
te
ri
al
d
er
m
at
it
is
;
n
eu
tr
o
p
h
il
ic
m
yo
ca
rd
it
is
;
n
eu
tr
o
p
h
il
ic
ly
m
p
h
ad
en
it
is
P
ro
b
ab
le
se
p
ti
ce
m
ia
an
d
b
ac
te
ri
al
m
yo
ca
rd
it
is
In
fe
ct
io
u
s
d
is
ea
se
(b
ac
te
ri
al
)
1
7
2
6
1
0
8
2
5
1
2
N
o
ve
m
b
er
1
9
9
7
A
M
B
ac
te
ri
al
m
yo
ca
rd
it
is
;
b
ac
te
ri
al
o
rc
h
it
is
;
d
is
se
m
in
at
ed
b
ac
te
ri
al
em
b
o
li
B
ac
te
ri
al
m
yo
ca
rd
it
is
,
o
rc
h
it
is
an
d
se
p
ti
ce
m
ia
In
fe
ct
io
u
s
d
is
ea
se
(b
ac
te
ri
al
)
MCFEE AND LIPSCOMB—PATHOLOGIC FINDINGS IN BOTTLENOSE DOLPHINS 579
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