Vet. Sci. 2015, 2, 407-422; doi:10.3390/vetsci2040407
OPEN ACCESS

veterinary sciences
ISSN 2306-7381
www.mdpi.com/journal/vetsci
Review

Atlantic Bottlenose Dolphins (Tursiops truncatus) as A Sentinel
for Exposure to Mercury in Humans: Closing the Loop
John S. Reif 1,*, Adam M. Schaefer 2 and Gregory D. Bossart 3
1

2

3

Department of Environmental and Radiological Health Sciences, Colorado State University,
Fort Collins, CO 80523, USA
Harbor Branch Oceanographic Institute at Florida Atlantic University, Fort Pierce, FL 34946, USA;
E-Mail: aschaef3@fau.edu
Georgia Aquarium, Atlanta, GA 30313, USA; E-Mail: gbossart@georgiaaquarium.org

* Author to whom correspondence should be addressed: E-mail: Jreif@colostate.edu;
Tel.: +1-970-491-6074.
Academic Editors: Peter M. Rabinowitz and Lisa A. Conti
Received: 14 October 2015 / Accepted: 5 November 2015 / Published: 12 November 2015

Abstract: Mercury (Hg) is a ubiquitous global contaminant with important public health
implications. Mercury is released from a variety of anthropogenic, industrial processes,
enters the earth's atmosphere and is re-deposited onto the earth’s surface in rainfall. Much of
this Hg enters the oceans which cover the majority of the earth’s surface. In the marine
environment, inorganic Hg is converted to the most toxic form of the element,
methylmercury, and biomagnified through the trophic levels of the food web. The bottlenose
dolphin (Tursiops truncatus) is the apex predator in many estuarine and coastal ecosystems.
Due to their long life span and trophic position, bottlenose dolphins bioaccumulate high
concentrations of contaminants including Hg, thus making them an important sentinel
species for ecosystem and public health. Bottlenose dolphins in Florida bioaccumulate high
concentrations of Hg in their blood, skin and internal organs. The concentrations of Hg in
blood and skin of bottlenose dolphins of the Indian River Lagoon, FL (IRL) are among the
highest reported world-wide. In previous studies, we demonstrated associations between
concentrations of total Hg in the blood and skin of IRL dolphins and markers of endocrine,
renal, hepatic, hematologic and immune system dysfunction. The predominant manifestation
of exposure to mercury in humans is neurotoxicity. During the 1950s and 1960s, residents
of Minamata bay, Japan were exposed to high concentrations of methyl mercury as the
result of ingestion of fish and shellfish that had become contaminated in this infamous

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environmental disaster. Affected adults had severe motor and sensory abnormalities often
leading to death. Methyl mercury crosses the placenta during pregnancy. Children exposed
in utero were born with multiple congenital anomalies and also suffered from neurologic
disorders. Significantly, local cats that consumed Hg contaminated fish developed severe
signs of neurotoxicity which led to their subsequent description as the “dancing cats of
Minamata bay”. Unfortunately, the cause of these strange manifestations in cats was not
recognized in time to prevent hundreds of additional cases from occurring. More recent
studies have shown that exposure to mercury as a result of seafood consumption during
pregnancy may result in multiple cognitive and neurodevelopmental effects in children.
The levels of mercury found in bottlenose dolphins and the health effects we identified
alerted us to the possibility of an important public health hazard. The IRL occupies
40 percent of the east coast of Florida and is bordered by counties with approximately
2.5 million human inhabitants. Therefore, we hypothesized that local inhabitants in
communities bordering the IRL could be at risk of exposure to Hg from the consumption of
fish and shellfish. We measured hair Hg in 135 local residents and found a mean
concentration of 1.53 µg/g which was higher than that from previous studies of sport
fishermen and coastal residents in other states. Over 50% of participants had a hair Hg
concentration which exceeded the U.S. EPA exposure guideline. Hair Hg concentration
was directly related to the frequency of seafood consumption and to the proportion of fish
and shellfish obtained from local recreational sources. This study clearly exemplifies the
importance of an animal sentinel in identifying a public health hazard and is virtually
unique in “closing the loop” between animal and human health.
Keywords: animal sentinels; bottlenose dolphins; epidemiology; fish; marine mammals;
mercury; one health

1. Introduction
Mercury (Hg) is a ubiquitous global contaminant with important public health implications.
Elemental and particulate-bound ionic forms of mercury are released into the environment from
multiple industrial processes such as metal production, waste incineration, mining and the burning of
coal for energy as well as natural phenomena such as volcanic eruptions [1]. Inorganic Hg enters the
atmosphere, is transported globally and is re-deposited onto the earth’s surface in rainfall and by dry
deposition [2]. Much of this re-deposited Hg enters the marine environment, primarily in the oceans,
which cover 71 percent of the earth’s surface. Inorganic Hg is converted to methylmercury (MeHg)
in aquatic sediments by the action of multiple anaerobic species of sulfate-reducing bacteria [3].
Thus the sulfate concentration and composition of bacterial communities in marine sediments are
important predictors of mercury methylation rates [4]. Methylmercury, in turn, is taken up from
sediments by phytoplankton and biomagnified through fish species within food webs, reaching the
highest levels in the apex predators within an ecosystem. Estuarine ecosystems, including the

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Everglades and much of southern Florida, are hydro-geological sinks for Hg due to their
biogeochemistry, concentrations of sulfates in sediments, pH and patterns of rainfall deposition [5].
2. Mercury Bioaccumulation in Dolphins
The Atlantic bottlenose dolphin (Tursiops truncatus) is an apex predator in many marine ecosystems.
They inhabit estuarine, coastal, and offshore waters along the Atlantic coast of the United States while
related species e.g., the striped dolphin (Stenella coeruleoalba) occupy the same ecologic niche in
other coastal waters such as the Mediterranean Sea. Due to their long life span and trophic position as
apex predators, bottlenose dolphins bioaccumulate high concentrations of organic and inorganic
contaminants including Hg, thus making them an important sentinel species for ecosystem and public
health [6–8].
It has long been recognized that deceased, stranded bottlenose dolphins from U.S. coastal waters
contain high levels of Hg in skin, liver, kidney and muscle [9–13]. Similar observations have been
made in coastal dolphins of various species in other hemispheres [14–17]. However, relatively few
studies have measured Hg in healthy, free-ranging individuals. The exceptions are from capture-release
health assessments conducted on the east and west coasts of Florida [18–21]. These studies were
conducted to establish baseline values for a suite of trace elements in populations from the Indian
River Lagoon (IRL) and Sarasota Bay, Florida. At both sites, high levels of total mercury (THg) were
reported in blood and skin obtained at the time of examination (Table 1). Dolphins captured between
2003 and 2005 in the IRL, a 165 mile estuary along Florida’s east-central coast, had mean concentrations
of THg of 658 ± 519 μg/L wet weight in blood [18], and 7.0 ± 5.9 μg/g dry weight in skin [19].
These concentrations were more than four times higher than those found in a comparison population of
bottlenose dolphins sampled in Charleston harbor, SC during the same time frame. Similar findings
were reported in bottlenose dolphins from the west coast of Florida where the concentration of THg in
blood was 570 ± 434 μg/L [20]. Approximately 73 percent of THg in the skin of dolphins from the
IRL was MeHg [19], while in Sarasota Bay dolphins 96% of the THg in blood was reported to be
MeHg [20].
Table 1. Reported concentrations of total mercury in blood and skin from bottlenose dolphins.
Study Site
Indian River Lagoon, FL
Charleston, SC
Sarasota Bay, FL
Sarasota Bay, FL
Italy, Aquaria
National Aquarium, Baltimore, MD

Years
2003–2005
2003–2005
2003–2005
2002–2004
2001
2011

Total Mercury Concentration Mean ± SD
Blood (μg/L ± SD)
Skin (μg/g ± SD)
658 ± 519.0 (n = 75)
7.0 ± 5.9 (n = 75)
147 ± 88.0 (n = 74)
1.7 ± 0.9 (n = 74)
570.3 ± 433.5 (n = 55)
2.1 ± 1.7 (n = 54)
512 ± 363 (n = 51)
2.13 ± 1.54 (n = 40)
139 ± 220 (n = 4)
63.9 ± 34.0 (n = 7)
-

Reference
[18,19]
[18,19]
[20]
[21]
[22]
[23]

Subsequently, mean concentrations of THg in the liver of stranded IRL dolphins were reported to be
10 fold higher than those found in stranded dolphins from South Carolina between 2000 and 2008 [13].
Further, a highly significant correlation was found between skin and liver concentrations of THg in
stranded dolphins from the IRL, documenting the usefulness of skin, a relatively accessible tissue in
live animals [13]. The concentration of THg found in wild Florida dolphins was approximately one

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order of magnitude greater than that found in dolphins in aquaria in Maryland and Italy, where the
concentration of THg in the fish diets were correspondingly lower [22,23]. The levels of THg in blood
and skin of Florida bottlenose dolphins are among the highest recorded in free-living marine mammals
worldwide. Collectively, these studies demonstrate that dolphins bioaccumulate high concentrations of
Hg in a variety of tissues as a result of biomagnification through trophic levels of the food chain.
3. The Indian River Lagoon, Florida
The Indian River Lagoon is a biodiverse estuary that occupies approximately 40% percent of the
east coast of Florida, spanning a distance of more than 250 km. The estuary has a narrow, linear shape
which dictates that dolphins essentially move along a north-south axis [24]. Bottlenose dolphins in the
IRL maintain strong site fidelity and have limited home ranges as shown by longitudinal photo-identification
studies of individual animals [25]. The estuary contains three major basins, and can be divided into
six segments based on unique hydrodynamic and geographic features. The IRL is connected to the
Atlantic Ocean by five inlets and one man-made canal, resulting in low rates of water turnover.
The shallow depth and the limited tidal exchange between the lagoon and the Atlantic Ocean results in
minimal flushing and concentration of microbial and chemical agents in the ecosystem [24].
We recently demonstrated a north to south gradient in THg blood concentrations in bottlenose
dolphins of the IRL by incorporating photo-identification data to assign individuals to geographic
segments [24]. Intense residential and urban population development and agricultural activity along
Florida’s east coast have resulted in increased freshwater inputs and altered water quality leading to
decreased seagrass habitat and eutrophication [26,27]. The northernmost areas of the IRL are relatively
pristine, while the southern segments are characterized by increased coastal development, greater
human population density and a higher concentration of drainage canals from inland areas [24].
These anthropogenic activities have impacted alkalinity, pH, and dissolved organic carbon concentrations
which can alter sulfate levels in sediments [28]. Elevated sulfate concentrations in the Florida Everglades
sediments increase the conversion rates of inorganic Hg to the methylated form which is bioaccumulated
in fish [29].
We also examined temporal trends in THg concentrations in blood of IRL dolphins [24]. From 2003
to 2012, the concentrations decreased significantly over time, consistent with decreases in THg in fish
species in the U.S. [30] and in striped dolphins from the Mediterranean Sea [16]. However, although
the linear trend in blood THg showed a significant decline between 2003 and 2012, most of the decline
was attributable to a high concentration in 2003 (1012 μg/L wet weight), which was between 20 and
58 percent lower and relatively stable between 2004 and 2012 [24]. The decline in Hg concentrations
in fish is attributed to reduction of exposure from point sources and emissions. However, trends in fish
in the southeastern United States between 1988 and 2005 (not including Florida) did not show the
decline found elsewhere in the country [30]. Deposition patterns show increases in this region and may
be due to a greater influence of global atmospheric Hg emissions, rather than local sources [30].
This appears to be the case for the IRL, since there are very few point sources of industrial activity
along the border of the lagoon. Rainfall deposition data also support this conclusion since over 50% of
Hg in south Florida is due to long range global transport of gaseous Hg and deposition rates remain
stable [31].

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4. Health Effects of Exposure to Mercury in Dolphins
Given the evidence that dolphins bioaccumulate high concentrations of Hg in a variety of tissues,
we explored the potential that this exposure may result in adverse patho-physiological effects on a
variety of organ systems. The study population consisted of 56 bottlenose dolphins from the IRL and
65 from Charleston Harbor, SC captured between 2003 and 2005 during the Bottlenose Dolphin Health
and Risk Assessment (HERA) project, a multidisciplinary collaborative effort designed to evaluate the
effects of environmental exposures on individual and population health [32]. We evaluated associations
between THg and selenium concentrations in blood and skin and endocrine, hepatic, renal and
hematological parameters using multiple linear regression models with adjustment for age in a pooled
analysis [33]. Selenium plays a protective role in mitigating the toxic effects of Hg through a variety of
mechanisms one of which is the formation of mercury-selenium complexes [34]. Recent research
demonstrates that selenium may operate through multiple mechanisms including competition with Hg
for biological targets, mobilization of mercury stores between organ systems and interactions in the
liver and kidney where MeHg is transformed into inorganic Hg [35,36]. Blood THg concentrations
were previously reported to be correlated with Se concentrations in IRL dolphins [18].
Increases in blood and skin THg concentrations were associated with a decrease in total thyroxine
(T4) and triiodothyronine (T3), demonstrating an effect on endocrine function [32]. In contrast,
adrenocorticotropic hormone (ACTH) increased with increasing concentrations of Hg in the blood and
skin. No statistically significant associations were found for free T4, testosterone, aldosterone, cortisol,
estradiol or progesterone. An effect on liver function was suggested by an increase in gamma-glutamyl
transferase (GGT) with increasing THg concentrations in blood and skin; lactic dehydrogenase was
positively correlated with skin THg. An effect on renal function was also found with an increase in
blood urea nitrogen (BUN) and increasing concentrations of THg in blood and skin; however, no
association was demonstrated for creatinine. With respect to hematological parameters, increases in
THg in blood and skin were associated with decreases in the absolute numbers of lymphocytes,
eosinophils and platelets and an increase in the absolute number of segmented neutrophils [33].
These results were consistent with previous reports. Associations between blood or skin Hg
concentrations and thyroid hormones, liver enzymes and several hematologic parameters were
described in a study of dolphins from Sarasota Bay, FL [20]. Pathologic changes in the liver consisting
of periportal lipofuchsin deposits, fatty infiltration, central lobular necrosis and lymphocytic
infiltration were described in dolphins from the west coast of Florida with high concentrations of Hg in
liver [37]. In summary, the results suggest the potential for a deleterious effect of Hg on the endocrine,
hepatic, renal and hematopoietic systems in highly exposed bottlenose dolphins.
We also studied the effects of increased exposure to Hg on the immune system of bottlenose
dolphins and found associations with both innate and acquired immunity, as well as with effects on
immune cell populations and immune globulins [38]. Data from 142 dolphins collected during the
HERA project from the IRL and Charleston Harbor, SC were analyzed by dividing Hg concentrations
in blood and skin into tertiles in a pooled analysis, adjusted for age. Total globulins increased
significantly across tertiles of blood Hg concentration due primarily to an increase in gamma globulin.
Two measures of innate immunity, monocyte phagocytic activity and plasma lysozyme concentration,
increased significantly with increasing concentration of blood Hg. Lymphocyte CD19 + (immature)

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and CD21 + (mature) B cell markers were reduced significantly. Non-significant reductions in CD2 +
and CD4 + helper T cell subpopulations were also observed. Antigen presenting cells expressing MHC
class II molecules decreased significantly with increasing categories of Hg exposure. B and T cell
lymphocyte proliferation were reduced in a stepwise, dose-dependent manner. Reductions in antibody
concentration to common marine micro-organisms suggested that dolphins with high exposures to Hg
may be more susceptible to infectious diseases [38]. Increased mortality from infectious disease
associated with Hg exposure was also reported in a study of cetaceans from the United Kingdom [39].
Mean liver concentrations of mercury, selenium and zinc were significantly higher in harbor porpoises
(Phocoena phocoena) that died of infectious diseases compared to healthy porpoises that died from
trauma [39].
Mercury is also known to cause immune system effects in humans [40]. Occupational exposures to
inorganic Hg were associated with alterations in B lymphocytes, T-helper cells, T-suppressor cells,
and T-cell proliferation. These findings led to the hypothesis that exposure to Hg increases risk for
infectious diseases in humans, subsequently supported by epidemiologic studies and laboratory based
research. Correlations between exposure to Hg and a self-reported history of malaria infections were
reported in Amazonian communities exposed through fish consumption in an area of alluvial gold
mining activity [41]. These populations also had changes in the serum concentration of antinuclear
antibodies (ANA) and antinucleolar antibodies (ANoA), biomarkers for autoimmune disease [42,43]
and in their profiles of pro- and anti- inflammatory cytokines [43]. Mercury has also been shown to
induce an autoimmune disease resembling lupus erythematosus in rodent models with increases in
immunoglobulins IgG and IgE [44], compatible with electrophorectic patterns in exposed dolphins.
5. Minamata Disease and Neurotoxicity of Methylmercury in Humans
A variety of health effects have been described in humans following exposure to organic and inorganic
Hg [40]. Principal among these is neurotoxicity, initially recognized through two well-documented
episodes. Severe neurologic impairment induced by the consumption of fish and shellfish containing
high levels of MeHg at Minamata Bay in Japan [45] was the initial harbinger of toxicity. In this well
chronicled environmental disaster, waste water discharges containing MeHg, produced as a byproduct
from the manufacture of acetaldehyde, were released from a chemical plant during the 1950s and 60s.
These discharges led to widespread contamination of the watershed, with high levels of organic Hg in
sediments, shellfish and fish [46]. Exposures to adults from consumption of seafood resulted in a
syndrome known as “Minamata Disease” characterized by symptoms of severe neurotoxicity; lack of
motor coordination, ataxia, muscle weakness, numbness, sensory disturbances, visual and hearing
deficits, seizures and death [45]. The ingestion of highly contaminated seafood by pregnant women
was followed by an epidemic of severe fetal abnormalities and neurotoxicity in their offspring.
Methylmercury crosses the placenta and the blood brain barrier, resulting in high levels in the
developing fetus [47]. These children exhibited congenital abnormalities such as microcephaly,
and were born with various central nervous system symptoms including blindness, seizures and severe
mental and physical developmental retardation [45]. A second large outbreak of neurotoxicity occurred
in Iraq in 1971–1972 as the result of consumption of bread made from methylmercury treated grain [48].

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Subsequently, more subtle neurodevelopmental effects have been demonstrated in cohort studies of
populations which rely heavily on the consumption of fish, shellfish and marine mammals as dietary
staples. Developmental neurotoxicity in children exposed prenatally was shown in cohort studies of
Faroese women who consumed a high proportion of their diet as seafood including meat from pilot
whales [49]. In a second large cohort study conducted in the Seychelles, the results were less clear
since the initial reports showed no association between maternal hair mercury and neurodevelopmental
test performance [50]. However, more recently, mercury was shown to have a negative effect in this
population when maternal fish consumption was taken into account in the analysis [51]. Similarly,
in a smaller U.S. cohort, maternal fish consumption was shown to improve performance on tests of
cognition in 6 months old children, while performance decreased with increased hair mercury
concentrations [52]. In general, low level exposure to mercury during pregnancy is associated with
decreased performance on tests of cognitive development and psychomotor performance in children
exposed in utero but the relationships are complex because of the beneficial effects of maternal fish
consumption [53,54]. Prenatal exposure can result in multiple cognitive and neurodevelopmental
effects including deficits in memory, language, attention, visual acuity and fine motor skills [52,55].
The prenatal exposure of children to MeHg derived from fish and seafood with resulting impaired
neurodevelopment is an important public health concern of international significance [40,56].
6. The Dancing Cats of Minamata Bay
The environmental disaster at Minamata bay included an animal sentinel, “the Dancing Cats of
Minamata Bay”. Not since the iconic description of “The Canary in the Coal Mine”, has the concept of
an early warning system for a human tragedy been so dramatically illustrated. Unfortunately, unlike
the miners who heeded the signs of carbon monoxide poisoning and went to the surface, the residents
of Minamata were unaware of the significance of events in the local cat population for at least
six years [45]. Although the effects of Hg intoxication were amply demonstrated in the animals of the
area, nothing was done to prevent or stop the human epidemic.
Harada [45] provides a vivid description. “During the 1950s, people began to witness strange
phenomena in and around Minamata Bay. For no apparent reason, fish rotated continuously and
floated belly-up to the surface, shellfish opened and decomposed, and birds fell while in flight.
The most shocking of all incidents was the frenzied death of cats. Cats suffered from excessive
salivation and manifested general convulsions or violent rotational movements, were unable to walk
straight, and often collapsed dead. Many jumped into the sea to drown, and eventually cats were no
longer seen in the area.” In retrospect, the explanation for the ataxic cats accompanied by convulsions
and death became clear. Local cats were fed fish and scraps of fish from the dinner tables of the
residents of Minamata [46]. Cats also provided confirmatory evidence of the role of MeHg in the
etiology of Minamata disease when laboratory analyses were later performed at Kumamoto University
(Table 2) [57]. High concentrations of THg in liver, kidney, brain and hair were found in cats from
Minamata compared to tissues from control cats obtained from a fishing village where no cases of
Minamata disease had occurred [46,57].

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Table 2. Concentrations of total mercury (ppm) in fish and shellfish and tissues from cats
and humans from Minamata Bay, Japan 1962. (Adapted from [57])
Fish and Shellfish
Oyster
5.6
Gray Mullet 10.6
Clam
20.0
China Fish
24.1
Crab
35.7

Cats
Control
0.9–3.66
Kidney 12.2–36.1
Liver
37–145.5
Brain
8–18.6
Hair
21–70

Humans
Control
<3.0
Kidney 3.1–144.0
Liver
0.3–70.5
Brain
0.1–24.8
Hair
96–705

A similar incident, albeit of much smaller proportions, occurred in Ontario, Canada in the 1960s
when a chloralkali plant released mercury into the river resulting in contamination of fish with MeHg.
At least one cat that consumed fish from the river developed a neurological disorder and toxicological
analysis of tissues from the cat confirmed Hg as the cause of the illness. Native Americans living in the
vicinity who consumed fish had high levels of mercury in hair samples [58].
7. The Bottlenose Dolphin as a Sentinel for Human Exposure
As described above, the Atlantic bottlenose dolphin is an apex predator in many marine ecosystems.
Bottlenose dolphins in the IRL are long-lived, bioaccumulate high concentrations of organic and
inorganic contaminants in blubber and other tissues and exhibit a relatively high degree of site fidelity,
making them an excellent sentinel animal for the potential health effects of environmental
contamination [8].
Human exposure to MeHg is primarily from the consumption of fish and shellfish [40]. While the
general population of the U.S. consumes most of its fish from commercial sources with resulting
relatively low levels of Hg in their tissues [59], sport fishermen and women appear to be a high risk
group for accumulation of MeHg. Studies of recreational fishermen in several states [60–62] have
demonstrated Hg concentrations in hair or blood above national averages and higher concentrations
among those who ate locally caught sport fish more frequently. Coastal subpopulations often consume
more fish and have higher concentrations of Hg in their tissues than the general population [63].
In Florida, the average adult consumes approximately 46 g per day of seafood, considerably higher
than the estimated 4.5 g per day for the general population in the United States [64].
The high concentrations of THg found in the blood and skin of bottlenose dolphins in the IRL
alerted us to the possibility of exposure to humans in the same area. The lessons learned at Minamata
Bay prompted us to undertake a study of Hg exposure among local residents along the IRL [65]. The IRL
is bordered by Brevard, Indian River, St. Lucie Martin and Palm Beach counties with a total population
of approximately 2.5 million full time residents. Therefore, we hypothesized that a substantial public
health problem might exist if the residents of these counties consumed locally caught seafood from the IRL.
We measured exposure to Hg among coastal residents living near the IRL to examine associations
between the frequency, species and sources of seafood consumed by residents and their hair Hg
concentration [65]. We enrolled residents of coastal counties bordering the IRL using an opportunistic
sampling design. Participants provided demographic information and were queried regarding their
consumption of fish and shellfish, the frequency and sources of their seafood consumption and the
frequency of consumption of 12 common sportfish. Participants provided a hair sample for the

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determination of THg. Hair has been validated as a reliable biomarker of Hg intake [66] and represents
total intake over the prior three months, the same period used in the food frequency questionnaire.
The mean THg concentration in hair for 135 residents was 1.53 µg/g. (Table 3) [65]. The U.S. EPA
exposure guideline, which equates to a hair Hg concentration of 1.0 µg/g [67], was exceeded in 50% of
participants. The hair Hg concentration among males (2.02 µg/g) was significantly higher than that for
females (0.96 µg/g). However, the concentrations in women of all ages in this study were approximately
five times higher than those from a randomly generated sample of U.S. women of childbearing age [68].
In addition, the concentrations of hair Hg in this study were higher than those reported from anglers
and coastal resident populations in Wisconsin (0.86 µg/g), Louisiana (1.1 µg/g) Alabama (0.55 µg/g)
and Canada (0.82 µg/g) [61,62,69,70].
Table 3. Concentrations of total mercury in hair (μg/g) among Florida residents, 2011–2012
by demographic and fish consumption variables (Adapted from [65]).
Participant Group
All Participants
Sex
Male
Female
Total Seafood Consumption
≥Once per day
Three times per week
Once per week
≤Once per month
IRL Seafood Consumption
≥Three times per week
Once per week
≤Once per month
Fish Sources
All locally caught
Most locally caught
Half locally caught
Most bought from store or restaurant
All bought from store or restaurant
Shellfish Sources
All locally caught
Most locally caught
Half locally caught
Most bought from store or restaurant
All bought from store or restaurant

n

Mean ± SD Median

Percentile
p-Value
75th 90th 95th
1.86 3.16 5.01
<0.01
2.81 4.74 6.06
1.38 1.98 2.60
<0.01
3.21
2.39 4.30 5.30
1.41 2.02 2.84
0.79 0.90
0.11
3.02
3.07 3.69
1.73 2.96 4.71
<0.01

135

1.53 ± 1.89

1.01

73
62

2.02 ± 2.38
0.96 ± 0.74

1.17
0.74

9
66
50
10

2.14 ± 1.86
1.95 ± 2.32
1.08 ± 1.16
0.49 ± 0.29

2.96
1.20
0.73
0.39

8
17
110

2.01 ± 1.47
1.71 ± 1.41
1.47 ± 1.99

1.19
1.14
0.89

28

2.53 ± 3.20

1.21

3.14

5.36

12.3

17
13
24
52

2.46 ± 2.24
1.65 ± 1.06
1.20 ± 0.71
0.85 ± 0.73

1.62
1.15
1.14
0.60

3.76
2.71
1.73
1.11

5.95
3.44
2.31
1.85

2.52
2.72
<0.01

14
10
5
19
85

3.37 ± 4.50
2.54 ± 1.83
2.77 ± 1.15
1.10 ± 0.82
1.12 ± 1.00

1.20
1.84
2.72
0.85
0.75

5.63
4.47
3.68
1.41
1.60

12.14
5.38
2.28
2.74

3.08

Hair Hg concentration was significantly associated with the frequency of total seafood
consumption. Individuals who reported consuming seafood once a day or more were almost four times
more likely to have a hair Hg concentration over the U.S. EPA reference dose, compared to those who

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consumed seafood once a week or less. Hair Hg concentration was also significantly higher among
individuals who obtained all or most of their seafood from local recreational sources [65].
Concentrations were highest among individuals who reported consuming seafood daily (2.14 µg/g)
and decreased with lower categories of total consumption (Table 3). Individuals who consumed
seafood from the IRL three times a week or more and those who reported that all fish and shellfish
consumed were from local recreational sources had the highest hair Hg concentrations (2.01 µg/g and
2.53 µg/g, respectively). Total hair Hg concentrations were significantly higher among individuals
who consumed snapper, sea trout, cobia, and grouper once a week or more compared to those who ate
these fish less than once a week [65]. A direct comparison of Hg contamination in fish consumed by
dolphins and humans was not undertaken since IRL dolphins consume a majority of their diet as
striped mullet, silver perch and spot [71].
8. Conclusions
Our recent study of coastal residents in Florida [65] marks the first investigation to apply findings
from bottlenose dolphins as a stimulus to explore the potential for similar risk among humans from the
same geographical region. Thus, by applying the knowledge gained from the study of this marine
mammal sentinel, we have “closed the loop” between animal and human health in a virtually unique
manner. In the general area of animal sentinels for human disease of non-infectious origin, very few
have linked the findings in the sentinel to a corresponding human exposure or health effect. One exception
is the seminal study of mesothelioma in the dog [72] in which asbestos exposure in the dog was linked
to occupational exposure or hobbies among the owners in most of the cases.
Following publication of the paper describing Hg exposure in humans in Florida [65], the topic
received considerable attention in the local media. There were more than 10 news stories on television,
radio and in local newspapers. These publications helped to raise awareness of potential risks of
consuming locally caught sportfish and shellfish, especially by pregnant women. Thus, we assume the
animal sentinel had a positive effect on public health through risk communication with members of the
local population. In a study conducted in Wisconsin, more than two thirds of the women who consumed
sportfish were not aware that fish consumption guidelines had been issued to protect against MeHg [63].
We are currently evaluating knowledge, attitudes and practices regarding the hazards of fish consumption
and exposure to Hg among pregnant women in Florida. This issue is timely in view of the fact that fish
consumption is widely recommended as a means of reducing the risk of cardiovascular disease due to the
high levels of n-3 polyunsaturated fatty acids present in the tissues of many species [73].
The current attention being devoted to Oceans and Human Health internationally [74] suggest that
additional studies of marine mammal sentinels should be conducted in a wide range of species and
locales. Multiple environmental challenges face the animals of the ocean and the humans who reside in
the vicinity or may be impacted indirectly. Animal sentinels may be useful in evaluating risks to
humans from climate change [75], harmful algal blooms [76], emerging chemical contaminants [77],
oil spills [78] and multiple other contemporary threats to ecosystem and public health.

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Acknowledgments
The authors thank the veterinarians, scientists, staff and volunteers who participated in the HERA
project. Tissues from HERA project dolphins were collected under National Marine Fisheries Service
Scientific Research Permits Nos. 998-1678 and 14352-03.
Author Contributions
All the authors included in this review article drafted the manuscript, which was revised by all
authors. All authors read and approved the final manuscript.
Conflicts of Interest
The authors declare no conflict of interest.
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