Environmental Pollution 214 (2016) 169e176
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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol
Mercury bioaccumulation in an estuarine predator: Biotic factors,
abiotic factors, and assessments of fish health*
Meredith S. Smylie a, *, Christopher J. McDonough b, Lou Ann Reed c,
Virginia R. Shervette d
a
Grice Marine Laboratory, College of Charleston, 205 Fort Johnson Road, Charleston, SC 29412, USA
Marine Resources Division, South Carolina Department of Natural Resources, 217 Fort Johnson Road, Charleston, SC 29422, USA
National Ocean Service, NOAA, Hollings Marine Laboratory, 331 Fort Johnson Road, Charleston, SC 29412, USA
d
Department of Biology and Geology, University of South Carolina Aiken, 471 University Parkway, Aiken, SC 29801, USA
b
c
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 26 January 2016
Received in revised form
29 March 2016
Accepted 1 April 2016
Estuarine wetlands are major contributors to mercury (Hg) transformation into its more toxic form,
methylmercury (MeHg). Although these complex habitats are important, estuarine Hg bioaccumulation
is not well understood. The longnose gar Lepisosteus osseus (L. 1758), an estuarine predator in the eastern
United States, was selected to examine Hg processes due to its abundance, estuarine residence, and top
predator status. This study examined variability in Hg concentrations within longnose gar muscle tissue
spatially and temporally, the influence of biological factors, potential maternal transfer, and potential
negative health effects on these fish. Smaller, immature fish had the highest Hg concentrations and were
predominantly located in low salinity waters. Sex and diet were also important factors and Hg levels
peaked in the spring. Although maternal transfer occurred in small amounts, the potential negative
health effects to young gar remain unknown. Fish health as measured by fecundity and growth rate
appeared to be relatively unaffected by Hg at concentrations in the present study (less than 1.3 ppm wet
weight). The analysis of biotic and abiotic factors relative to tissue Hg concentrations in a single estuarine
fish species provided valuable insight in Hg bioaccumulation, biomagnification, and elimination. Insights
such as these can improve public health policy and environmental management decisions related to Hg
pollution.
© 2016 Elsevier Ltd. All rights reserved.
Keywords:
Methylmercury
Trophic ecology
Longnose gar
Lepisosteus osseus
1. Introduction
Mercury (Hg) is a naturally occurring metal and its aerial
deposition rate has increased at least threefold since the 19th
Century due in part to anthropogenic activities (Biester et al., 2002;
Bindler et al., 2001). In many species of animals its organic form,
methylmercury (MeHg), affects sensorimotor systems in utero and
in adults. While the harmful effects of acute Hg exposure are well
documented for humans (Mahaffey, 1999; Watanabe and Satoh,
1996), the potential effects at environmental concentrations for
other animal species are less studied (Basu et al., 2005; Friedmann
et al., 1996). Mercury concentrations among individuals within a
*
This paper has been recommended for acceptance by Harmon Sarah Michele.
* Corresponding author. Current address: Greeley Memorial Laboratory, Yale
University, 370 Prospect Street, New Haven, CT 06511, USA.
E-mail address: [email protected] (M.S. Smylie).
http://dx.doi.org/10.1016/j.envpol.2016.04.007
0269-7491/© 2016 Elsevier Ltd. All rights reserved.
species can be highly variable across spatial and temporal gradients
and with respect to an individual's size, sex, and diet (Adams and
Onorato, 2005; Bank et al., 2007; Tremain and Adams, 2012).
Examining this variability across multiple populations within a
single species allow for further insights into the factors that influence Hg bioaccumulation rates (Adams and Onorato, 2005; Adams
and Paperno, 2012; Eagles-Smith and Ackerman, 2014; Tremain
and Adams, 2012).
Estuaries serve as a connection between terrestrial ecosystems,
freshwater environments, and the open ocean; therefore, estuarine
Hg concentrations can be influenced by all three. Within estuaries,
wetlands are major contributors to the transformation of inorganic
Hg into its most toxic and bioaccumulative form, MeHg, by sulfurand iron-reducing bacteria as well as methanogens (Kerin et al.,
2006; Kim et al., 2008; St. Louis et al., 1996; Wood et al., 1968).
Estuaries are also important nursery and foraging grounds for
resident and transient biota (Shervette et al., 2004, 2007; Witting
et al., 1999) and are important for fisheries and recreational
170
M.S. Smylie et al. / Environmental Pollution 214 (2016) 169e176
activities for humans (Barbier et al., 2011). As a result, Hg
contamination may have profound effects on the ecology and
biology of estuarine organisms, as well as human health, though
estuarine Hg bioaccumulation patterns remain poorly understood
(Glover et al., 2010). Further elucidation of the spatial and temporal
effects of Hg on estuarine biota is necessary for assessing risks to
animals and humans.
Many studies have examined the influence of biotic factors on
Hg in fish and have demonstrated that fish size is strongly correlated with Hg concentrations. For this reason fish size is often
length-normalized in order to detect variation driven by other
factors (Barbosa et al., 2011; Burger et al., 2001; Murphy et al., 2007;
Petre et al., 2012; Sonesten, 2003; Szczebak and Taylor, 2011; Ward
and Neumann, 1999). Additionally, only a few studies have
compared concentrations between sexes and of those, results were
inconsistent regarding differences in Hg levels between male and
female fishes (de Pinho et al., 2002; Farmer et al., 2010; Murphy
et al., 2007; Nicoletto and Hendricks, 1988; Ward and Neumann,
1999). Differences in Hg concentrations between sexes could be
attributed to different energetic costs for reproduction, growth
dilution (Karimi et al., 2007), distinctions in habitat use, or a
combination of these. Mercury levels can also change due to animal
movement for spawning or feeding if an animal migrates to an area
which is contaminated more or less than its area of origin (AlMajed and Preston, 2000). Despite the level of existing knowledge, the relationship between Hg and biotic factors within estuaries remain poorly understood.
At any given time, the Hg concentration in an organism reflects
the net accumulated Hg, which represents the amount gained from
the environment and the organism's rate of elimination. Relatively
little work has focused on Hg elimination because it is difficult to
measure, especially in field studies (Van Walleghem et al., 2013;
Van Walleghem et al., 2007); however, Trudel and Rasmussen
(1997) summarized that the half-life of MeHg ranges between
130 and 1030 days within long-term experiments on fishes. Evidence for maternal transfer, one elimination mechanism, of Hg has
been described in a number of spawning fishes (Alvarez et al., 2006;
Hammerschmidt and Sandheinrich, 2005; Hammerschmidt et al.,
1999; Johnston et al., 2001; Sackett et al., 2013) and could
contribute to low Hg concentrations in adulthood. This however
has not previously been documented in estuarine species.
The longnose gar Lepisosteus osseus, (L. 1758) was selected for
studying Hg bioaccumulation given its abundance and ubiquity in
estuarine systems within the eastern United States and its importance as an upper trophic level predator (Smylie et al., 2015). This
species thrives in fresh water rivers and lakes, but can tolerate
brackish and marine salinities (Goodyear, 1967; Henzler, 2011;
Hildebrand and Schroeder, 1928; McGrath, 2010). Longnose gar
are large, gonochoristic, and opportunistic predators (Smylie et al.,
2015) with high reproductive output and a long life span (McGrath,
2010; Smylie et al., 2016). Growth is rapid until sexual maturity
(Netsch and Witt, 1962), which occurs at approximately one year of
age for males and six years for females in South Carolina (Smylie
et al., 2016). Females generally have larger body sizes and attain
greater ages than males, though studies have produced inconsistent results regarding growth rate between the sexes (Kelley, 2012;
Klaassen and Morgan, 1974; Netsch and Witt, 1962; Smylie et al.,
2016). Despite its relative abundance, the life history of the longnose gar is poorly understood. The daily and seasonal movement
patterns are largely unknown, though it is believed that longnose
gar move to saline waters at night to feed, return to fresh water
during the day (Goodyear, 1967) and cross large distances to spawn
upstream in late spring and early summer (McGrath et al., 2012;
Netsch and Witt, 1962; Smylie et al., 2016).
A better understanding of factors determining Hg levels in
estuarine fishes is important because of the inherent complexity in
estuarine environments and because humans closely interact with
these systems. To provide a more comprehensive knowledge of
factors influencing Hg bioaccumulation patterns within estuarine
fishes, the objectives of this study were to: 1. Summarize total Hg
levels in estuarine populations of longnose gar along spatiotemporal gradients; 2. Describe the relationships between Hg concentration and fish size, sex, and age; 3. Determine if variability in
Hg concentration relates to trophic position, as measured by C and
N stable isotope signatures; 4. Examine how Hg concentration
correlates with measures of fish health; and 5. Evaluate the potential for maternal Hg transfer in this species.
2. Materials and methods
2.1. Study area
Mercury methylation rates vary among ecosystems (Benoit
et al., 2002; Gilmour and Henry, 1991; Gilmour et al., 1992; King
et al., 1999). Although the underlying mechanisms for this remain
poorly understood, several studies have demonstrated that dissolved organic carbon levels in the water, water pH, and the
abundance of sulfur-reducing bacteria play a role (Gilmour and
Henry, 1991; Gilmour et al., 1992; Miskimmin, 1991). Coastal
South Carolina is characterized by turbid estuaries containing
extensive wetlands and Spartina alterniflora (Loisel.) salt marshes.
The abundant vascular plant material along waterways can
decompose aerobically and anaerobically. The anaerobic processes
are driven by bacteria and contribute to the transformation and
biogeochemical cycling of many nutrients and pollutants (Dame
et al., 2000). Two SC estuarine systems, the Winyah Bay/Pee Dee/
Black River system and the Charleston Harbor/Wando/Cooper/
Ashley River system (Dame et al., 2000), were sampled to examine
Hg bioaccumulation patterns of coastal longnose gar. Winyah Bay
flows from a 45,163 km2 watershed influenced by agricultural and
industrial production and excessive decomposing organic material
(Dame et al., 2000; Guentzel and Tsukamoto, 2001). Charleston
Harbor Estuary has a small drainage of about 900 km2 and is
composed of the Ashley, Cooper, and Wando (Knott and Martore,
1991) rivers which converge around Charleston, SC. This estuary
also contains several small ponds including Schultz Lake. For this
study, longnose gar were collected from these two estuarine systems, with opportunistic samples collected from Schultz Lake, and
Lake Moultrie (Fig. S1).
2.2. Sample collection
Longnose gar were collected from May 2012 through July 2013
by South Carolina Department of Natural Resources (SCDNR) from
two fishery-independent coastal monitoring programs: the
trammel-net survey and the electrofishing survey (Arnott et al.,
2010). These programs are monthly randomly stratified surveys of
seven estuaries (strata), two of which (Ashley River and Winyah
Bay, SC) were selected for this study. The electrofishing survey was
used to complement the trammel-net survey by sampling the
brackish and tidal fresh water regions where trammel nets were
not effective. Additional longnose gar were obtained as bycatch
from another SCDNR monitoring program using electrofishing to
sample large striped bass Morone saxatilis (Walbaum 1792) in the
Schultz Lake headwaters of the Ashley River from March through
April 2013 and by gillnetting opportunistically in Lake Moultrie, SC.
A maximum of ten longnose gar from 100-mm-total length size
classes (1e1199 mm) were collected from both estuarine systems
per month with approximately half coming from each sampling
method. At each capture site, water temperature and salinity were
M.S. Smylie et al. / Environmental Pollution 214 (2016) 169e176
recorded using a handheld YSI meter (YSI Inc., Yellow Spring, OH).
Specimens were brought to the laboratory for immediate processing and euthanized according to American Veterinary Medical Association (Leary et al., 2013) guidelines. Total and standard length
(SL) were measured to the nearest mm, and sex was determined
visually then verified histologically (Smylie et al., 2016). Sagittal
otoliths were removed, rinsed, and stored dry for later age determination and gonads were either preserved in 10% seawaterbuffered formalin before histological preparation or frozen prior
to Hg quantification. Muscle fillets were removed from the left
anterior part of the body excluding ribs, and then frozen until
analyzed. Stainless steel cutlery was used to remove the fillets and
was sterilized according to South Carolina Department of Health
and Environmental Control fish processing standard operating
procedure (SCDHEC, 2001).
2.3. Reproduction
For confirmation of sex and determination of maturity, gonad
tissue was processed using standard methodology for histological
paraffin embedding and hematoxylin and eosin-y staining
(Humason, 1967). A full description of methods used for the histological determination of maturity and reproductive phases is
available in Smylie et al. (2016).
To examine the potential for maternal transfer of Hg, ovary and
muscle subsamples were taken from reproductively active longnose gar collected from Lake Moultrie in February 2013. Prior to
sample processing, oocytes were carefully removed from connecting tissue to ensure that all measured Hg was within germ
tissue.
2.4. Health assessment
Fecundity was estimated gravimetrically from mature females
captured from November 2012 through July 2013. Ovarian tissue
was divided into six sections: proximal, medial, and distal for each
ovary (Smylie et al., 2016). Three of these sections were randomlyselected as subsamples from each individual. Subsamples weighed
one to two percent of total gonad weight and were removed, rinsed
with water, and stored in 70% alcohol until the large, vitellogenic
oocytes were counted.
To evaluate growth, sagittal otoliths were embedded in epoxy
resin and sectioned (0.4e0.6 mm thick) longitudinally through the
nucleus, which is located near the distal-anterior edge, using a low
speed saw with a high-concentration diamond-edged blade.
Otolith sections were mounted on glass slides and examined with a
dissecting microscope (30) using transmitted light. Increments
(one translucent and one opaque zone) were counted by two independent readers with no reference to fish size or date of capture.
Observed individual lengths at age were fitted to the Von Bertalanffy growth function (von Bertalanffy, 1938) (Eq. (1)):
Lt ¼ L∞ 1 ekðtt0 Þ
(1)
where Lt is length at time of capture, L∞ is estimated maximum
attainable length, k is the growth parameter, t is time (age), and t0 is
time (age) at which Lt is equal to zero.
2.5. Stable isotope analysis
For d13C and d15N stable isotope analysis, a subsample of fish
(n ¼ 39) were selected from samples collected in the Ashley River
system between March and June of 2012 and 2013. From these fish,
muscle biopsies were removed, frozen, and lyophilized for at least
171
24 h. Samples were then ground with a mortar and pestle into a fine
powder which was transferred into tin capsules and analyzed in a
Delta V Plus Isotope mass spectrometer at the Skidaway Institute
Scientific Stable Isotope Laboratory in Savannah, GA. Shrimp chitin
powder standard was used as a control for isotopes of both elements. Results of analysis were given as deviations from chitin
standards using the following formula (Eq. (2)):
dX ¼
Rsample
1 103
Rstandard
Where X is 13C or
(Craig, 1953).
15
N and R is either the
(2)
13
C/12C or
15
N/14N ratio
2.6. Mercury analysis
Mercury concentrations were determined using a DMA-80
Direct Mercury Analyzer (Milestone Inc., Shelton, CT) to quantify
the total mercury (THg) within an approximately 0.3 g subsample
of thawed fillets and oocytes. Because MeHg is the predominant
form of Hg in muscle tissues (Bloom, 1992), THg was measured as a
proxy for MeHg. Two to three blanks, two dogfish liver tissue
(DOLT-3), and one oyster tissue (1566b) reference material samples
were run prior to tissues samples, after every nine samples, and
after the final sample to ensure accuracy of results and limit THg
carryover between high concentration samples. In addition,
approximately 20% of muscle fillet samples were run in duplicate or
triplicate to measure precision. Relative standard deviation (%RSD)
was calculated for all samples run as multiples and samples
exceeding 10% were excluded from analyses. Calibration curves had
r2 values exceeding 0.99. The percent of recovery of DOLT-3 fell
within 85 and 115% and analysis of blanks showed no substantial
levels of THg. All reported data were within the range of calibrated
values.
2.7. Statistical analysis
All statistics were run using natural log-transformed tissue Hg
concentrations to correct not normally distributed data. To test the
null hypothesis that no significant difference existed in muscle Hg
concentrations among months of fish capture, a one factor ANOVA
was used, followed by a Bonferroni post-hoc comparison to detect
pairwise differences between months. A linear regression was used
to quantify the relationship between muscle Hg concentrations and
salinity. A t-test was used to compare mean muscle Hg concentrations between estuaries.
To compare mean Hg levels between the sexes, a Wilcoxon rank
sum test was used. A two factor ANOVA was used to test for differences in Hg relative to reproductive stage and sex followed by
Bonferroni post-hoc tests to detect pairwise differences between
reproductive stages for each sex, excluding regenerating females
(n ¼ 1). Fourier polynomial regressions were used to independently
assess relationships between muscle Hg levels and fractional age or
SL using sex as a covariate. Relationships between d13C and d15N
and Hg concentration were tested using linear regressions.
In order to determine if fish with relatively high muscle Hg
concentrations exhibited lower length at age relationships, samples
were categorized as low Hg (<0.25 ppm) and high Hg (>0.25 ppm)
(Friedmann et al., 1996). Because length-at-age relationships were
significantly different between the sexes (Netsch and Witt, 1962),
the low and high Hg groups were further divided between the sexes
and length-at-age was estimated for these four groups using the
Von Bertalanffy growth model. The growth parameters were then
compared between low and high Hg levels for males and females
using c2 tests to determine if Hg affected the length at age
M.S. Smylie et al. / Environmental Pollution 214 (2016) 169e176
Mercury concentrations differed significantly among months
(df ¼ 11, F ¼ 3.54, p < 0.001). The Bonferroni post hoc test indicated
that mean muscle Hg in August was significantly lower compared
to March, April, May, and June (Fig. 1). Mercury in fillets was
inversely related to salinity (r2 ¼ 0.11, df ¼ 344, p < 0.001; Fig. 2).
Between the two estuaries, mean Hg concentrations in muscle
were significantly higher in the Ashley River than Winyah Bay
(t ¼ 2.10, df ¼ 295, p < 0.05).
Males had significantly higher mean Hg levels than females
(W ¼ 10,955, p < 0.001) though females have been shown to grow
larger and older than males (Netsch and Witt, 1962). Reproductive
phase was a significant factor with respect to fillet Hg concentration
(F-Ratio ¼ 8.23, p < 0.001) with a significant sex interaction (FRatio ¼ 4.90, p < 0.005). Bonferroni post hoc tests revealed
significantly greater Hg in immature males than spawning capable
males (p < 0.05; Fig. S2a) and significantly greater Hg in immature
females compared to all other stages (p < 0.01; Fig. S2b). As a result
of the differences in Hg between sexes, relationships between Hg
levels in muscle and SL and fractional age were tested including sex
as a covariate. Fractional age had a significant, though weak,
parabolic relationship with THg (F-Ratio ¼ 11.05, df ¼ 2339,
r2 ¼ 0.06, p < 0.05; Fig. 3a) with a significant sex effect (p < 0.05)
while SL also had a significant, parabolic relationship with THg (FRatio ¼ 15.71, df ¼ 3342, r2 ¼ 0.11, p < 0.001; Fig. 3b) with no
significant sex effect (p ¼ 0.73). With respect to trophic position,
THg in muscle was negatively associated with d13C (Fstatistic ¼ 28.47, df ¼ 38, r2 ¼ 0.41, p < 0.001; Fig. 4a) and d15N (Fstatistic ¼ 16.74, df ¼ 38, r2 ¼ 0.29, p < 0.001; Fig. 4b).
Muscle Hg was positively associated with fecundity (tau ¼ 0.185,
p < 0.05; Fig. S3). Length at age relationships significantly differed
between longnose gar with high and low THg concentrations for
males and females (Males: p < 0.001, Females: p < 0.001; Fig. 5).
The relationship between muscle fillet Hg levels and those in oocytes from the same individuals was also significant (df ¼ 15,
F ¼ 33.73, r2 ¼ 0.67, p < 0.001; Fig. 6).
Hg Concentration (ppm)
3. Results
1.4
1.2
1
0.8
0.6
0.4
0.2
0
0
10
20
Salinity (ppt)
30
40
Fig. 2. Scatterplot of Hg concentrations and salinity for longnose gar captured in the
Charleston Harbor and Winyah Bay estuaries in South Carolina from May 2012 through
July 2013.
1.4
a
Females
1.2
Hg Concentration (ppm)
relationship in SYSTAT (Systat Software Inc, 2014). We tested for
maternal transfer of Hg into oocytes by comparing muscle and
oocyte Hg concentrations with a linear regression. Unless otherwise stated, analyses were performed in R (R Development Core
Team, 2014). Results were considered significant when p < 0.05.
Males
Unknown
1
0.8
0.6
0.4
0.2
0
0
1.4
Hg Concentration (ppm)
172
5
10
15
Fractional age
20
25
Females
1.2
30
b
Males
Unknown
1
0.8
0.6
0.4
0.2
0
0
Hg Concentration (ppm)
0.35
a
0.3
0.25
0.2
ab
ab
a
a
a
ab
ab
ab
b
ab
ab
0.15
0.1
200
400
600
800
Standard Length (mm)
1000
1200
Fig. 3. Mercury concentrations by fractional ages (a) of male and female longnose gar
captured from the Charleston Harbor and Winyah Bay estuaries in South Carolina from
May 2012 through July 2013. The solid and dashed parabolic fit lines represent male
(y ¼ 0.0028x20.0412x þ 0.3921) and female (y ¼ 0.0015x20.0344x þ 0.3848) Hg at
age respectively. Mercury levels and standard lengths (b) of male and female longnose
gar.
The
solid
and
dashed
parabolic
fit
lines
represent
male
(y ¼ 2 1006x20.0025x þ 0.924) and female (y ¼ 1 1006x20.0016x þ 0.7705)
Hg at age respectively. Parabolic curves were selected based on least squared residuals.
0.05
0
Fig. 1. Monthly mean Hg and standard error for longnose gar captured in the
Charleston Harbor and Winyah Bay estuaries in South Carolina from May 2012 through
July 2013. Letters above denote significant differences among months.
4. Discussion
To our knowledge, this study was the first to examine Hg concentration trends along temporal and salinity gradients a priori
within two discrete populations of a single species and the first to
use longnose gar as an indicator of Hg levels in estuarine top
predators. Unlike the majority of other fishes investigated,
M.S. Smylie et al. / Environmental Pollution 214 (2016) 169e176
a
1
0.8
0.6
0.4
0.2
700
600
500
400
300
-30
-25
-20
-15
-10
-5
Male High Hg
200
Male Low Hg
100
0
0
-35
a
800
Hg Concentration (ppm)
1.2
900
Standard Length (mm)
1.4
173
0
0
5
10
Fractional Age
δ13C
b
1.2
20
b
1200
1000
Standard Length (mm)
Hg Concentration (ppm)
1.4
15
1
0.8
0.6
0.4
0.2
800
600
400
Female High Hg
200
Female Low Hg
0
5
10
δ15N
15
20
Fig. 4. Mercury concentrations and d13C (a) and d15N (b) isotopic signatures for
longnose gar captured in the Charleston Harbor estuary, SC from March through June
(2012/2013).
longnose gar appear to not bioaccumulate Hg in linear or exponential processes with ontogeny, and instead have highest concentrations in early life stages. This pattern of decreasing Hg
concentrations with ontogeny could be attributed to Hg-associated
mortality, Hg elimination, or growth dilution. We found evidence of
maternal transfer, a contaminant elimination mechanism, at low
concentrations, though implications for juvenile health, fish
recruitment success, and development remain unclear. These
concentrations were also too low to account for the magnitude of
Hg loss from juvenile stages to adulthood.
Similar to other studies, muscle Hg decreased with increasing
salinity within the estuary (Farmer et al., 2010; Glover et al., 2010).
The transformation and bioavailability of MeHg are dependent on
the abundance of sulfate and the associated sulfate-reducing bacteria (Choi and Bartha, 1993; Compeau and Bartha, 1985; Devereux
et al., 1996; King et al., 1999). In lower salinities, sulfate is limiting
and Hg methylation occurs readily where it is present (Choi and
Bartha, 1994). In higher salinities, sulfate is abundant and forms
mercury-sulfide complexes, which inhibit methylation. As a result,
MeHg is often negatively correlated with sulfide concentrations
and salinity (Benoit et al., 1999). The significant difference in
average Hg levels between the two estuaries may have been the
result of differences in sampling effort. In general, longnose gar
smaller than 500 mm TL were caught primarily in freshwater regions while larger specimens were collected in all salinities. Along
the Ashley River, which is part of the Charleston Harbor Area,
sampling efforts in the lower salinity regions were more robust,
which increased the number of samples collected in fresher,
possibly more Hg contaminated areas, as well as the number of
small fish with high Hg concentrations. In contrast, within Winyah
Bay, a smaller area was sampled relative to the watershed size and
0
0
5
10
15
Fractional Age
20
25
30
Fig. 5. Length at age relationships for high (>0.25 ppm) and low (<0.25 ppm) Hg
concentrations for males (a) and females (b). Fit lines are dashed for low Hg fish.
0.07
Oocyte Hg Concentration (ppm)
0
0.06
0.05
0.04
0.03
0.02
0.01
0
0
0.1
0.2
0.3
0.4
0.5
Muscle Hg Concentration (ppm)
0.6
0.7
Fig. 6. Oocyte Hg concentrations relative to maternal muscle Hg levels in longnose gar
from Lake Moultrie, South Carolina in February 2013.
the size range of longnose gar collected was narrower. Therefore,
the higher mean Hg concentration in the Ashley River could be
inflated because of these sampling differences.
Mercury in muscle tissue also varied temporally within the two
estuaries. Average Hg levels in longnose gar were higher in spring
than any other time of year which has also been demonstrated in
other fishes (Farmer et al., 2010; Murphy et al., 2007; Ward and
Neumann, 1999). Murphy et al. (2007) speculated that this trend
could be the result of increases in bioavailability, increased feeding
rates, changes in tissue composition during this time of year, or a
combination of these factors. The feeding rate of longnose gar from
this study was highest during autumn (Smylie et al., 2015),
174
M.S. Smylie et al. / Environmental Pollution 214 (2016) 169e176
suggesting that the Hg peak in spring may be driven more by
environmental bioavailability or metabolic changes influencing the
muscle composition rather than feeding rate. Muscle tissue
composition also changes seasonally. Lipid content is typically
lowest in spring and winter (Adams et al., 1993; Ward and
Neumann, 1999); therefore, Hg concentration may increase during this time due to the muscle having a greater proportion of
protein.
In this study, males had higher muscle THg concentrations than
females. Other studies have documented significant differences in
sex-specific Hg tissue concentrations (Murphy et al., 2007;
Nicoletto and Hendricks, 1988) while others have not (Farmer
et al., 2010; Ward and Neumann, 1999). Differences in Hg concentrations between the sexes have generally been attributed to a
combination of factors such as differences in growth rate, longevity,
and energetic budgets which also vary among species (Farmer et al.,
2010; Murphy et al., 2007; Nicoletto and Hendricks, 1988; Ward
and Neumann, 1999). The significantly higher mean Hg level in
immature females compared to other females was likely driven by
greater early life exposure to Hg in the fresh water environment.
Immature males had the highest mean Hg concentration relative to
other males, though this was only significantly higher than
spawning capable individuals. The pronounced spike in mean Hg
within regressing males may be driven by acute Hg exposure and
an increased feeding rate in fresh water or a decrease in muscle
lipid content around the time of spawning (Adams et al., 1993;
Murphy et al., 2007; Ward and Neumann, 1999). Additionally, the
frequency of each reproductive phase depends on the time of year;
therefore, the average Hg concentration for each reproductive
phase is dependent on seasonal environmental and biological
fluctuations.
Most previous research has shown a net increase in Hg concentration with increasing size or age within freshwater and marine fishes (Barbosa et al., 2011; Murphy et al., 2007; Petre et al.,
2012; Szczebak and Taylor, 2011; Ward and Neumann, 1999). The
weak parabolic relationship between muscle Hg and size in this
species does not appear to reflect the typically strong trend of linear
or exponential Hg increase with size seen in other species. Instead,
the absence of a strong predictive relationship between length and
Hg in the muscle of longnose gar may indicate that this species can
eliminate Hg more effectively and therefore their tissue concentrations may reflect Hg exposure levels within a relatively short
time scale.
In the present study, longnose gar appeared to have high early
life exposure to Hg through maternal transfer and environmental
conditions. They also exhibit a loss of Hg from early life stages into
adulthood, though this trend reversed in older and larger individuals (Fig. 3). This finding suggests that longnose gar, in
contrast to most fishes for which data exist, may eliminate Hg more
readily, which could explain the decrease in Hg from early life into
early adulthood. Maternal transfer of organic Hg (Johnston et al.,
2001), one elimination mechanism, has not previously been
demonstrated in gar species. An alternative explanation to elimination is that existing Hg in the body becomes less concentrated as
the organism grows through a disproportional increase in biomass
compared to Hg uptake: a process known as biodilution (Karimi
et al., 2007). The increase in Hg in older adults could be driven by
a decreased Hg elimination rate in larger and older fish. Trudel and
Rasmussen (1997) attempted to model Hg elimination in fishes
using existing literature and found a negative correlation between
Hg elimination rate and body size.
Diet is the primary pathway for Hg uptake in fishes (Van
Walleghem et al., 2013) and in the present study, d13C and d15N
were negatively related to Hg (Fig. 4). The carbon isotope signature
reflects the carbon source, or primary producers at the base of the
food web. Aquatic areas with higher flow, such as pelagic zones and
upriver areas, generally have more negative d13C values than
benthic or downriver areas because C13 is more readily taken up in
areas with lower water movement (Deegan and Garritt, 1997; Doi
et al., 2005; France, 1995). As a result, d13C variation reflects differences in foraging location and carbon source. In this study,
ontogenetic changes in d13C were likely driven predominantly by
differences in feeding location along the river rather than differences in the depth preferences of prey consumed. Increases in d13C
values with ontogeny corresponded to a transition from benthic to
pelagic prey and to larger individuals generally residing downriver
(Smylie et al., 2015). Other studies have documented a positive
relationship between d15N or its proxy, trophic level, and Hg (Bank
et al., 2007; Burger et al., 2001; Watras et al., 1998). Bank et al.
(Bank et al., 2007) compared Hg relative to d13C and d15N for gray
and red snapper in coastal Louisiana and found d15N to explain the
majority of the Hg variation between the two species, though a
model combining d13C and d15N was the best model for predicting
Hg levels in both species. In the present study, d13C was found to be
a slightly better, though still a poor predictor of Hg concentration
compared to d15N which indicated that spatial distributions of Hg
sources (prey) may have a greater influence on Hg exposure than
trophic level in estuaries.
Mercury concentration in fish muscle was not significantly
related to measures of fish health. We found a weak but positive
relationship between Hg concentration and female fecundity
(Fig. S3). While Hg concentration did not increase with size
throughout ontogeny, it did increase with size in the older, reproductively capable individuals for which fecundity was estimated.
This increase in Hg with body size in older, larger individuals may
be the driving factor for the positive association between fecundity
and Hg. These findings may suggest that the Hg levels documented
in longnose gar were not high enough to result in negative reproductive effects. Negative reproductive effects have been detected in
walleye at concentrations as low as 0.25 ppm (Friedmann et al.,
1996) showing that Hg sensitivity could vary among species.
Length-at-age was significantly lower for male and female individuals with higher Hg concentrations (Fig. 5). This may indicate
that Hg negatively impacts growth. Friedmann et al. (1996)
examined the impact of dietary Hg on growth in juvenile walleye
and found growth impairment at concentrations seen in wild
populations. The relationship between growth rate and Hg concentration is complex because these variables are capable of
influencing each other (Friedmann et al., 1996; Trudel and
Rasmussen, 2006). Growth rate, degree of dietary Hg exposure,
and the ratio of growth to consumption rate change throughout
ontogeny which complicates attempts to model Hg bioaccumulation with respect to size and growth (Trudel and
Rasmussen, 2006).
5. Conclusions
The present study found a suite of biotic and abiotic factors
which influenced Hg concentrations found within this top predator.
Salinity and d13C largely varied spatially and these variables were
strongly correlated with muscle Hg concentration. This finding has
ramifications for studying Hg exposure in other estuarine fish
populations as estuarine use varies among species as well as
ontogeny and time of year. The anomalous relationship between Hg
concentrations and fish size and age in longnose gar suggests
movement coupled with ontogenetic shifts to a more saline foodweb may have driven Hg levels in fish tissue in unexpected ways.
Also these results suggest that knowledge of the trophic ecology of
fishes that inhabit transitional areas like estuaries is essential to
better understand the complex pathways of Hg in our environment
M.S. Smylie et al. / Environmental Pollution 214 (2016) 169e176
and the levels in fish tissue. Additionally, the high concentrations in
early life stages were above consumption advisory limits set by the
Environmental Protection Agency (USEPA, 1997); therefore, the
concept of humans consuming smaller fish to reduce risk of Hg
toxicity (Burger et al., 2001) may not apply to all fish species.
Length-at-age was significantly smaller in fish with high Hg levels
which could have significant influence on fishes with high early life
exposure to Hg, such as those which spawn in freshwater. Having a
more comprehensive understanding of the spatial distribution, life
history patterns, and uptake and elimination rates of species of
interest is crucial to making informed decisions regarding risks to
fishes, fisheries management, and the humans that may consume
them.
Conflict of interest disclosure
All procedures performed in studies involving animals were in
accordance with the ethical standards of the institution or practice
at which the studies were conducted. This article does not contain
any studies with human participants performed by any of the
authors.
This publication does not constitute an endorsement of any
commercial product or intend to be an opinion beyond scientific or
other results obtained by the National Oceanic and Atmospheric
Administration (NOAA). No reference shall be made to NOAA, or
this publication furnished by NOAA, to any advertising or sales
promotion which would indicate or imply that NOAA recommends
or endorses any proprietary product mentioned herein, or which
has as its purpose an interest to cause the advertised product to be
used or purchased because of this publication.
Acknowledgements
This paper originated from the Master's thesis of MSS and the
project idea was developed initially by VRS and MSS. MSS collected
all the data for this paper and wrote it with the assistance and
guidance of VRS who was her thesis advisor. CJM and LAR were part
of the thesis committee and contributed to this paper through
assistance with chemical analysis, data analyses and interpretation,
and important editorial guidance and feedback.
Thanks to the Inshore Fisheries and Mariculture Divisions of the
SCDNR for sample collection, Jay Brandes for providing instruction
during stable isotope processing, and Bill Roumillat and Patrick
Biondo for help with reproductive histology. Funding for this work
came from: US Dept. of Energy through the Nuclear Workforce
Initiative of the SRS Community Reuse Organization (VRS), University of South Carolina Aiken Dept. of Biology and Geology (VRS),
and The Joanna Deep Water Fund Fellowship (MSS). This is
contribution number 747 from the Marine Resources Research
Institute of the SCDNR.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.envpol.2016.04.007.
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