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Metal concentrations in coastal sharks from The Bahamas with a focus on the Caribbean Reef shark


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Over the last century anthropogenic activities have rapidly increased the influx of metals and metalloids entering the marine environment, which can bioaccumulate and biomagnify in marine top consumers. This may elicit sublethal effects on target organisms and have broad implications for human seafood consumers. We provide the first assessment of metal (Cd, Pb, Cr, Mn, Co, Cu, Zn, As, Ag, and THg) and metalloid (As) concentrations in the muscle tissue of coastal sharks from The Bahamas. A total of 36 individual sharks from six species were evaluated, spanning two regions/study areas, with a focus on the Caribbean reef shark (Carcharhinus perezi), and to a lesser extent the tiger shark (Galeocerdo cuvier), due their high relative abundance and ecological significance throughout coastal Bahamian and regional ecosystems. Caribbean reef sharks exhibited some of the highest metal concentrations compared to five other species, and peaks in the concentrations of Pb, Cr, Cu, Zn, and Ag were observed as individuals reached sexual maturity. Observations were attributed to foraging on larger, more piscivorous prey, high longevity, as well a potential slowing rate of growth. We observed correlations between some metals, which are challenging to interpret but may be attributed to trophic level and ambient metal conditions. Our results provide the first account of metal concentrations in Bahamian sharks, suggesting individuals exhibit high concentrations which may potentially cause sublethal effects. Finally, these findings underscore the potential toxicity of shark meat and have significant implications for human consumers.
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Scientic Reports | (2021) 11:218 | 
Metal concentrations in coastal
sharks from The Bahamas
with a focus on the Caribbean Reef
Oliver N. Shipley1*, Cheng‑Shiuan Lee1,2, Nicholas S. Fisher1, James K. Sternlicht3,
Sami Kattan3, Erica R. Staaterman3, Neil Hammerschlag4 & Austin J. Gallagher3
Over the last century anthropogenic activities have rapidly increased the inux of metals and
metalloids entering the marine environment, which can bioaccumulate and biomagnify in marine top
consumers. This may elicit sublethal eects on target organisms, having broad implications for human
seafood consumers. We provide the rst assessment of metal (Cd, Pb, Cr, Mn, Co, Cu, Zn, As, Ag, and
THg) and metalloid (As) concentrations in the muscle tissue of coastal sharks from The Bahamas.
A total of 36 individual sharks from six species were evaluated, spanning two regions/study areas,
with a focus on the Caribbean reef shark (Carcharhinus perezi), and to a lesser extent the tiger shark
(Galeocerdo cuvier). This is due their high relative abundance and ecological signicance throughout
coastal Bahamian and regional ecosystems. Caribbean reef sharks exhibited some of the highest
metal concentrations compared to ve other species, and peaks in the concentrations of Pb, Cr, Cu
were observed as individuals reached sexual maturity. Observations were attributed to foraging on
larger, more piscivorous prey, high longevity, as well a potential slowing rate of growth. We observed
correlations between some metals, which are challenging to interpret but may be attributed to trophic
level and ambient metal conditions. Our results provide the rst account of metal concentrations in
Bahamian sharks, suggesting individuals exhibit high concentrations which may potentially cause
sublethal eects. Finally, these ndings underscore the potential toxicity of shark meat and have
signicant implications for human consumers.
Over the past century, anthropogenic activities such as rapid industrialization, smelting, and fossil fuel combus-
tion have signicantly increased the concentration of metals and metalloids (herein metals) entering marine
environments1. Many metals (e.g., Cr, Cu, and Zn) are introduced into marine systems via freshwater inputs,
euent run-o, weathering, and ocean–atmosphere interactions2,3. Although essential metals such as Cr, Cu,
and Zn are required at low concentrations to support healthy cellular processes, many can become toxic when
they exceed threshold concentrations4,5. ese eects may cause sublethal impacts in aquatic organisms such as
delayed growth, reproductive impairment, and greater incidence of disease6,7 and may have carcinogenic and
neurotoxicological impacts for humans8. Most metals bioconcentrate and a few biomagnify in marine organisms
once they enter the ocean3,9,10. Accordingly, long-lived, large-bodied marine predators that exhibit higher trophic
positions oen display potentially toxic concentrations of metals and other toxicants1114,and can therefore be
used as environmental sentinels for regional loadings1517. As many higher trophic-level marine shes comprise
a proportion of the global seafood demand, a need exists to monitor metal concentrations and evaluate the
potential toxicity risk for humans readily consuming sh protein8,16,17.
Metal concentrations are typically evaluated in higher-order, commercially important shes to mitigate
potential toxic eects on humans; this concern has led to widespread monitoring and scientic study8,1820.
However, for higher order predators of historically low commercial value, such as sharks, assessments are much
sparser. Sharks are medium to large-bodied predators that occupy meso-to-apex trophic positions throughout
marine food-webs2123 and as a result are intrinsic to healthy ecosystem function and resilience24,25. Despite the
      
           Beneath the
      Rosenstiel School of Marine and Atmospheric Science, University of
 *email:
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historically low commercial value of shark meat, relative demand as a human protein source appears to be a
growing global trend26. A need to establish baseline concentrations of metals in sharks and their relatives, as
well as potential routes of exposure is therefore required14,17,20. is is particularly true for developing nations,
where less stringent environmental regulations regarding wastewater treatment, anthropogenic emissions, and
subsequent management may lead to elevated levels of metals entering coastal waters.
e developing nation of e Bahamas houses a diversity of productive marine ecosystems such as seagrass
beds, oolitic sand banks, open ocean, coral reefs, and mangroves27. is high productivity supports biomass of
upper trophic level predators, such as sharks, and large teleost shes28,29. High shark diversity and abundance in
this region stems from over two decades of legislated protection: commercial long-lining was banned in 199330,31,
and the Bahamian EEZ was declared a ‘shark sanctuary’ in 2011, thereby prohibiting the capture, harvest, or
trade of shark products within the exclusive economic zone31,32. However, the highly migratory nature of coastal
sharks33,34 may increase sheries capture and eventual human consumption as a protein source in other neighbor-
ing regions of the Greater Caribbean. Baseline monitoring of metal concentrations is therefore necessary to exam-
ine the primary route/s of metal exposure and establish the potential toxicity of shark meat. Ultimately, this will
allow for the determination of potential hotspots that may benet from focused environmental management16.
is study provides the rst assessment of metal (Cd, Pb, Cr, Mn, Co, Cu, Zn, Ag, Hg) and metalloid (As)
concentrations in muscle tissue of large-bodied, common shark species from the coastal Bahamas. We present
preliminary concentrations for ve species: blacknose sharks (Carcharhinus acronotus), bull sharks (Carcharhinus
leucas), tiger sharks (Galeocerdo cuvier), nurse sharks (Ginglymostoma cirratum), and lemon sharks (Negaprion
brevirostris). However, we focus much of our analyses on the Caribbean Reef shark Carcharhinus perezi3537 owing
to their high abundance, ecological signicance on Bahamian coral reefs, and high capture rate in neighboring
regions where they remain unprotected from shing and human consumption (e.g., South American sheries38).
We also examined correlations between metal concentrations across individuals and examined trends with size.
ese ndings establish the rst baseline estimates of metal concentrations in Bahamian sharks with broader
implications for the human consumption of shark meat and allow for preliminary inferences regarding the
ultimate route/s of metal exposure for these species.
Metal concentrations in muscle tissue were measured for 36 individuals spanning six species (Table1). Most
sharks sampled were mature based on established size-at-maturity estimates (Compagno etal. 2005), but for
Caribbean reef sharks we were able to sample individuals across a broader size range. Total mercury (THg)
concentrations were up to 1.5 times higher in Caribbean Reef sharks (16.490 ± 8.331mgkg−1; mean ± SD) than
in any other species and these values were higher than those reported in most other sharks species that are
commonly found and sampled from e Bahamas and neighboring regions (Table2). Despite their larger size,
tiger sharks exhibited the lowest THg concentrations of all species (4.442 ± 1.619mgkg−1, Table1), and these
results were statistically signicant when comparing Caribbean Reef sharks and Tiger sharks (Wilcoxon test,
W = 6.000, p < 0.001, Fig.1).
e highest concentrations of Cd were found in the tissues of Nurse sharks (0.263 ± 0.301mgkg−1) and Lemon
sharks (0.231 ± 0.170mgkg−1) and the lowest values were found in Caribbean reef sharks (0.119 ± 0.085mgkg−1).
The highest concentrations of Pb were found in Caribbean reef sharks (0.367 ± 0.231 mgkg−1). For
Cr, the highest values were observed in Caribbean reef sharks (2.641 ± 3.272 mg kg−1) and blacknose
sharks (2.577 ± 2.156 mgkg−1). Manganese and cobalt concentrations were highest in blacknose sharks
(Mn = 1.515 ± 1.396 mgkg−1, C o = 0.042 ± 0.073mg kg−1) and tiger sharks (Mn = 1.765 ± 1.938 mgkg−1,
Co = 0.047 ± 0.033 mg kg−1). Cu concentrations were up to five times higher in lemon sharks
(30.877 ± 25.443mgkg−1) than in any other species sampled (< 6.5mgkg−1). Zn concentrations were highest
in blacknose sharks (104.168 ± 114.608mgkg−1) and nurse sharks (88.004 ± 28.582mgkg−1). In some spe-
cies, As concentrations were up to two times higher in Caribbean reef sharks (7.307 ± 19.287mgkg−1) than in
the other species sampled (< 9.000mgkg−1). Ag concentrations were over four times higher in lemon sharks
(0.518 ± 0.408mgkg−1) than in the other species sampled (< 0.120mgkg−1).
We observed strong, positive correlations (r > 0.4) between many of the metals measured within the muscle
tissues of Caribbean reef sharks (Table3, Fig.2). Cd concentrations were positively correlated with Co, and
negatively correlated with THg. Pb concentrations were positively correlated with Cr, Mn, Cu, Zn, As, and THg.
Cr concentrations were positively correlated with Mn and Co. Mn concentrations were positively correlated with
Cu, Zn, As, and THg. Co concentrations were positively correlated with Ag. Cu concentrations were positively
correlated with Zn. Zn concentrations were positively correlated with As and THg. Finally, signicant positive
correlations were observed between concentrations of As and THg (Table3, Fig.2). We observed a negative
correlation between THg and Cd.
Generalized additive models revealed variable trends in metal accumulation with size (Table4, Fig.3) for
Caribbean reef sharks. For three of the metals (Pb, Cr, and Cu) there appeared to be signicant increases in con-
centrations as individuals approached sexual maturity (152–168cm45; 150–170cm46); a relatively high percentage
of the total deviance was also explained by these models (> 39%, Table4). Trends for Mn, Co, Zn, As, and Ag
were less conspicuous, with little or no trend observed. For THg, GAMs revealed a positive, linear relationship
with size (Table4, Fig.3).
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Table 1. Mean heavy metal concentrations (± SD, mg kg−1, dw) measured in white muscle tissue of sharks
captured from coastal waters of Great Exuma and Nassau New Providence Island, e Bahamas. Sample sizes
(n) represent the total number of individuals sampled from which metal data were generated, the sample sizes
of individual metals may dier based on the removal of data due to potential contamination. a n = 4. b n = 4.
c n = 3. d n = 6. e n = 21. f n = 19. g n = 23. h n = 2.
Species Common
name Size range
(TL, cm) nCd Pb Cr Mn Co Cu Zn As Ag THg
shark 97–114 3 0.151
(0.028) 0.104
(2.156) 1.515
(1.396) 0.042
(0.073) 4.227
(1.686) 104.168
(114.608) 2.576
(3.860) 0.067
(0.047) 7.908
nus perezi Caribbean
reef shark 94–197 24 0.119
nus leucas Bull shark 242 1 0.216 0.142 0.09 0.16 0.534 2.73 37 1.38 0.055 6.722
cuvier Tiger shark 155–320 7 0.138
cirratum Nurse shark 204–267 5 0.263
(0.301) 0.108
(1.112) 0.640
(0.313) 0.009
(0.019) 6.411
(4.412) 88.004
(28.582) 3.750
(3.909) 0.094
(0.126) 9.030
brevirostris Lemon
shark 240, 248 2 0.231
(0.170) 0.125
(0.108) 2.305
(2.553) 0.467
(0.217) 0.010
(0.014) 30.877
(25.443) 64.140
(37.640) 0.306
(0.432) 0.518
(0.408) 4.846
is study represents the rst evaluation of metal concentrations in large-bodied sharks from e Bahamas.
e high and variable concentrations of metals in the muscle tissue of coastal sharks in this region exceeded
concentrations considered toxic for human consumption (e.g., THg8). Considering the demand for shark meat
worldwide47, our data provide baseline concentrations of metals and further emphasize the potential toxicity of
shark meat for human consumers8,48,49. Despite the potential implications for humans, we focus our discussion on
the potential drivers of metal concentrations in sharks, and why these may vary across and within taxa. We found
that Caribbean reef sharks exhibited the highest concentrations in four of metals (Pb, Cr, As, and THg) relative
to other larger-bodied species, some of which peaked as animals approached sexual maturity. We also found
Table 2. Summary of literature-derived total mercury (THg) concentrations (mg kg−1, wet weight) reported
for shark muscle tissue in species typically found throughout e Bahamas and neighboring regions (updated
and adapted from Matulik etal. 2017). Concentrations for sharks captured in this study were converted to wet
weight by multiplying dry weight concentrations by 0.3 assuming a ~ 70% moisture content reported for shark
muscle tissue44.
Species n Mean Range/SD Sampling location Study
Carcharhinus limbatus 21 0.77 0.16–2.3 Florida, US 39
Carchahinus leucas 53 0.77 0.24–1.7
Carcharhinus limbatus 5 1.9 1.44–2.73 Unknown 40
Carcharhinus spp. 9 1.61 0.46–4.08 Gulf of Mexico, US 41
Carcharhinus acronotus 11 1.76 SD: ± 0.8
Florida, US 12
Carcharhinus limbatus 28 2.65 SD: ± 0.9
Carcharhinus leucas 7 1.48 SD: ± 1.2
Nepagrion brevirostris 2 1.67 and 1.69
Sphyrna mokkarran 4 1.65 SD: ± 0.4
Galeocerdo cuvier 8 0.37 SD: ± 0.3
Carcharhinus acronotus 8 2.93 1.65–4.90
Florida, US 42
Carcharhinus leucas 7 3.95 1.89–7.43
Carcharhinus limbatus 23 3.22 1.20–5.99
Nepagrion brevirostris 8 1.28 0.85–2.40
Carcharhinus longimanus 24 5.04 1.86–11.20 Cat Island, Bahamas 43
Carcharhinus acronotus 3 2.37 1.84–2.89
New Providence Island and Great Exuma, Bahamas is study
Carcharhinus perezi 24 4.65 1.11–1.72
Carcharhinus leucas 1 2.02
Galeocerdo cuvier 7 1.33 0.73–1.93
Ginglymostoma cirratum 5 2.71 1.23–3.54
Nepagrion brevirostris 2 1.45 1.38–1.52
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some signicant (both positive and negative) correlations between metal concentrations in this species, which
could be attributed to foraging dynamics, longevity, physiology, and a slower growth rate in older individuals.
A notable nding was the elevated metal concentrations in Caribbean reef sharks, particularly THg, relative
to the other larger-bodied species sampled and values reported for other coastal sharks sampled from neigh-
boring regions (see Table2). Species-specic dierences in bioaccumulation trajectories of toxicants have been
reported in sharks12,50, whereby variable physiologies, trophic ecologies, and maternal ooading may inuence
the initial concentrations and subsequent bioconcentration42,51. One explanation for the generally high metal
concentrations in Caribbean reef sharks could be ascribed to a piscivorous diet in larger individuals, foraging
upon predominantly larger coral reef-associated shes (e.g., Grouper, Snapper, and Barracuda), which exhibit
Figure1. Total mercury concentrations (mg kg−1, DW) in the tissues of tiger (n = 6) and Caribbean Reef sharks
(n = 23) sampled from the coastal waters of e Bahamas. Asterisk indicates statistical signicance at α = 0.05.
e median sizes of sharks sampled was 162cm for Caribbean reef sharks* and 301cm for tiger sharks. *Note
that median length estimates for Caribbean reef sharks are based o n = 22 as a single individual that was
measured for THg was DOA and could not be accurately measured for TL.
Table 3. Correlation coecients (p value) for Spearman’s correlation tests examining relationships between
trace metal concentrations in the muscle tissue of Caribbean Reef sharks. Bold indicates statistically signicant
correlation at α = 0.05 level. Sample sizes for each specic comparison are shown in the second horizontal.
Cd Pb Cr Mn Co Cu Zn As Ag THg
Cd n = 19 n = 21 n = 21 n = 21 n = 21 n = 21 n = 21 n = 21 n = 20
Pb −0.076 (0.758) n = 19 n = 19 n = 19 n = 19 n = 19 n = 19 n = 19 n = 18
Cr −0.030 (0.897) 0.664 (0.002) n = 21 n = 21 n = 21 n = 21 n = 21 n = 21 n = 20
Mn −0.187 (0.418) 0.731 (< 0.001) 0.661 (0.001) n = 21 n = 21 n = 21 n = 21 n = 21 n = 20
Co 0.510 (0.018) 0.323 (0.178) 0.465 (0.034) 0.311 (0.170) n = 21 n = 21 n = 21 n = 21 n = 20
Cu −0.076 (0.743) 0.732 (< 0.001) 0.768 (< 0.001) 0.503 (0.020) 0.266 (0.243) n = 21 n = 21 n = 21 n = 20
Zn −0.141 (0.543) 0.820 (< 0.001) 0.487 (0.025) 0.548 (0.010) 0.110 (0.634) 0.669 (0.001) n = 21 n = 21 n = 20
As −0.257 (0.261) 0.426 (0.069) 0.244 (0.286) 0.386 (0.084) −0.284 (0.213) 0.438 (0.047) 0.696 (< 0.001) n = 21 n = 20
Ag 0.060 (0.796) 0.214 (0.379) 0.376 (0.093) 0.003 (0.991) 0.137 (0.553) 0.396 (0.076) 0.194 (0.400) 0.367 (0.102) n = 20
THg −0.529 (0.016) 0.548 (0.018) 0.162 (0.494) 0.457 (0.043) −0.233 (0.323) 0.334 (0.150) 0.408 (0.075) 0.334 (0.150) −0.162 (0.496)
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Figure2. (A) Box and whisker plots highlighting the distribution of measurements for metals (mg kg−1, DW).
Solid horizontal line represents the median, box limits are 1st and 3rd quantiles, whiskers are 1.5 times the
interquartile range, and circles represent outliers. (B) Correlograms highlighting Spearman’s correlation tests
assessing covariance between trace metal concentrations in Caribbean Reef sharks. Circles represent signicant
correlations at alpha = 0.05 level, size of circles scales with size of correlation (i.e., larger circles indicate higher
correlation coecient) coecient and colors ramp illustrates whether correlations are positive (blue) or negative
(red). See Table2 for sample sizes associated with each statistical comparison. Correlograms were created in the
R package “corrplot” (Wei and Simko, 2017).
Table 4. Deviance explained (%) by generalized additive models between size and metal concentrations for
Caribbean Reef sharks.
Metal Deviance explained (%)
Cd 8.3
Pb 42.6
Cr 39.6
Mn 37.8
Co 4.25
Cu 48.3
Zn 14.4
As 0.6
Ag 30
THg 28.8
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high metal concentrations at other Bahamian locales (e.g., South Eleuthera52). For THg, the remarkably high
concentrations reported here exceed those in nearly all other marine animals17,53, which may be ascribed in
part to diet54,55but also to ambient oceanographic conditions specic to sub-tropical waters such as high ocean
temperatures (which increase methylation rates of inorganic Hg by marine microbes56). is may explain the
higher THg concentrations in less mobile sharks either known or assumed to display high residency within
Bahamian waters (e.g., Caribbean reef sharks36; blacknose sharks and nurse sharks), relative to more transient
species that move throughout much of the northern Western Atlantic ocean, such as tiger sharks33,34. Although
it remains unknown if high THg concentrations in Caribbean reef sharks elicit neurological eects, there are
human health concerns as this species is commonly consumed in certain regions of the Caribbean57, as well as
in South America38. Because THg concentrations were high across multiple species sampled in this study, fur-
ther evaluation of local euent and runo of Hg sources into Bahamian marine systems is certainly warranted.
is argument is strengthened by observations of elevated concentrations reaching 0.8ppm (WW) for THg,
which have been observed in teleost species such as king mackerel (Scomberomorus cavalla) and great barracuda
(Sphyraena barracuda) from neighboring waters of South Eleuthera52.
Very few studies have explored correlations between metal concentrations in sharks, and trends are oen
inconsistent among species possibly due to variable metabolisms14,51,58. Bosch etal.8 found no correlation among
metals in smoothound sharks (Mustelus mustelus), whereas Kim etal.59 found a signicant relationship between
Figure3. Generalized additive models (GAMs) t for Caribbean Reef sharks investigating relationships
between size and metal concentrations (mg kg−1, dw). Blue shaded region represents standard error and blue
dotted region represents range of published size-at-maturity estimates (152–168 cm45; 150–170cm, Pikitch
etal.46). Sample sizes dier between metals owing to removal of data that were potentially contaminated.
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Hg and Pb in copper sharks (Carcharhinus brachyurus). In this study, we found that zinc and manganese were
positively correlated with lead, arsenic and mercury in the muscle of Caribbean reef sharks. It is thus possible
that these micronutrient metals have some protective eects against heavy metal toxicity60,61. Metal competition
(e.g., competition for metal binding sites) could lead to negative correlations62,63, whereas similar accumula-
tion behaviors, detoxication processes, and similar input sources could result in positive correlations64,65. For
example, it is suggested that metallothioneins induced by elevated Zn and Cu can interact with and detoxify
metal ions such as Cd, Hg, Pb, and Ag60,61. Here, we did not observe signicant, positive correlations for Zn–Cd
and Cu–Cd, but positive correlations were found for Zn–Pb, Zn–Cu, Zn–Hg, and Cu–Pb. Similarly, we found
positive correlations between Pb and most of the metals (except Cd, Co, and Ag), implying they might be intro-
duced into the study area though similar geochemical pathways (e.g., dust deposition for Pb and Mn, metal-rich
particulate/organic matter from runo or suspended sediment). Although the ultimate cause and implications
of metal correlations are challenging to establish for wild sampled sharks, our descriptive approach indicates
that direct experimental study assessing the biological and environmental factors that drive metal correlations,
or lack thereof is warranted.
We observed size-based shis in concentrations of Pb, Cr, Cu, and THg in Caribbean Reef sharks, which
peaked as animals reached sexual maturity (Belize: 150–170cm46). Indeed, for Pb, Cr, and Cu. is observa-
tion could be explained by a resource-use shi from inshore habitats to deeper continuous reefs35, running
parallel to deep slopes of the Tongue of the Ocean (near our Nassau, New Providence sampling region) from
juvenile/sub-adult to mature life-history stages. is behavior may thus present a dierent prey base11, or ambi-
ent concentrations of metals in the water column (i.e., if the primary pathway of metal accumulation is through
the gills). As sharks reach sexual maturity, energetic requirements associated with reproduction may increase
overall daily energy budgets44, requiring individuals to consume a greater biomass of potentially higher trophic
position prey items. Although we were unable to denitively test this hypothesis within the connes of this
study, ecogeochemical tracer techniques such as stable isotope and fatty acid analyses may provide insight into
whether resource-use shis are in fact occurring between size classes. In other shark species, such as tope sharks
(Galeorhinus galeus) shis in metal concentrations have been attributed to habitat shis11, but it is apparent that
trends are not uniform across all metals, tissue types, and species. Combined, this suggests that factors other than
the organisms ecology may play a role in the accumulation of metals. For example, metabolic processes, such as
reduced growth rates may lead to greater metal accumulation in Caribbean reef shark tissues as processes such
as growth dilution are signicantly reduced53.
e study provides the rst analysis of metal concentrations in the tissues of coastal sharks from e Bahamas.
e higher trophic position of the shark assemblage sampled in this study may partly explain why concentrations
were elevated. For Caribbean reef sharks, we found the highest levels of harmful THg compared with the other
species sampled. We also found peaks in metal concentrations as this species reached sexual maturity, which
could be associated with the known ontogenetic shi in habitat/primary prey base combined with growth dilu-
tion eects. We recognize that obtaining larger sample sizes should improve comparisons across species, and
arm that there are limitations for interpreting some of the relationships detected here due to knowledge gaps
in our understanding of metal trophodynamics in elasmobranch shes. Overall, our ndings suggest that sharks
residing within relatively pristine ecological environments may possess high levels of potentially harmful met-
als, which may have public health implications if they are consumed by local human populations. Further, our
ndings suggest that Bahamian food-webs may support elevated concentrations of toxic metals and although
e Bahamas legally protects sharks from shing, sublethal impacts may still be induced. As such, future work
should seek to determine the habitat-level sources and assimilation factors of metals in sharks and whether
overall tness is aected by high tissue concentrations.
Animal ethics statement. All research was conducted under scientic research permits issued to A. Gal-
lagher (unnumbered) by e Bahamian Department of Marine Resources. Animal handling and sampling pro-
tocols followed guidelines listed by the Association for the Study of Animal Behavior65. Ethical approval for
animal sampling was given by the Canada research chair for animal care (Carelton University, Ottawa, Canada).
Animal capture and tissue sampling. Sharks were sampled from the coastal waters of Nassau, New
Providence and Great Exuma between February 2018 and February 2019 (Fig.4) using standardized circle-hook
research drum lines. Upon capture, animals were secured alongside the research vessel and sex and morphomet-
ric measurements were taken. A small incision was made into the dorsal musculature using a sterilized scalpel
and approximately 1–2g of white muscle tissue was excised using a modied 10mm biopsy punch (Deglon,
iers, France). All samples were frozen on ice in 2mL microcentrifuge tubes in the eld and then stored
−20°C before preparation for elemental analysis. Samples were oven dried at 60°C for ~ 48h and ground to a
ne powder using a mortar and pestle. For statistical purposes, all Caribbean reef shark samples were pooled
because capture locations are consistent between islands (e.g., lagoon and forereef habitat), and we cannot dis-
count the movement of individuals between islands.
Analyses of metals and metalloids. Total mercury (ppm, mg kg−1) analysis was conducted on a Mile-
stone DMA-8-Direct Mercury Analyzer. Machine error calculated from repeat measurements of certied refer-
ence material (DORM-4) fell within expected ranges (0.412 ± 0.036mgkg−1). e remaining trace metals (Cr,
Mn, Co, Cu, Zn, As, Ag, Cd, and Pb) were analyzed by a sector eld double focusing high-resolution inductively-
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coupled plasma mass spectrometer (HR-ICP-MS, Element 2, ermo Fisher Scientic). Tissue samples were
digested into liquid prior to analysis. In brief, a small amount (10 ~ 20mg) of tissue was soaked in 1mL of nitric
acid (70%, trace metal grade, Fisher Chemical) in a metal-free polypropylene vial at room temperature overnight.
Aer adding 1mL of hydrogen peroxide (30%, trace analysis, Supelco), the vial was sealed and heated at 90°C
for 12h until complete digestion. e digest was then combined with Milli-Q water to obtain samples in 2%
nitric acid solution which were ready for ICP-MS analysis. 114Cd and 208Pb were measured in the low-resolution
mode, while 52Cr, 55Mn, 59Co, 63Cu, 66Zn, 75As, and 107Ag were measured in the medium-resolution mode. Inter-
nal standards 115In and 89Y were used for correcting potential matrix interference. e accuracy of the standard
calibration was validated with the certied reference material, Trace Metals in Water Standard A (CRM-TMDW-
A, High-Purity Standards). e mid-point standard and the blank were checked every twelve measurements to
correct instrumental dris of the background and the slope of the calibration curve. Two random digest samples
were fortied with a known quantity of elements, and the recovery of each spiked element ranged from 74 to
97% (Supplementary TableS1). e certied reference material of sh tissue, DORM-4 (NRCC), was used to
ensure the accuracy of the digestion and analytical procedure, which fell within certied ranges (Supplemen-
tary TableS2). e instrument detection limit for each metal is listed in Supplementary TableS3. Data above
the limit of detection (LOD) were presented. e few samples that exhibited anomalous metal concentrations
indicative of contamination were removed from the analyses which are likely to have occurred randomly during
subsampling or transportation in the eld. e concentration range of each metal presented in this study was
comparable to other common shark species reported in earlier literature8,11 though the shark species may dier).
Note that we reported the concentration on a dry weight basis and the metal concentration would drop 60–80%
as converted to wet weight44.
Statistical analyses. All data were analyzed in the statistical programming soware R (version 4.0.0). Sta-
tistical signicance α was 0.05. Shapiro–Wilks tests and F tests were used to examine normality and hetero-
scedasticity of data, respectively. For Caribbean reef sharks, we examined potential correlation between trace
metals through Spearman’s correlation coecients, presented as correlograms (R package “corrplot”66. We used
a rank order Spearman’s correlation because some values fell below detection limits and are therefore expressed
as zeros. A Wilcoxon signed ranks test was used to examine whether mean THg concentrations statistically dif-
fered between Caribbean reef sharks and tiger sharks; low sample sizes for other species and metals precluded
comparisons between other species. We also compiled literature derived THg concentrations for shark muscle in
species found throughout the Bahamas and neighboring waters for comparative purposes. Because relationships
between size and metal concentrations are not necessarily linear, we investigated these using generalized additive
models (GAMs, R package “mgcv”67). e smoothing parameter k was set to 9 to ensure sucient degrees of
Figure4. Sampling location of sharks from Great Exuma (black boxes, top le panel) and Nassau New
Providence Island (red boxes, bottom le panel), e Bahamas in relation to North Americas and wider
western Atlantic Ocean (right panel). Sources: ESRI, GEBCO, NOAA, National Geographic, DeLorme, HERE,, and other.
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freedom to represent a trend and this parameterization was validated using the ‘gam.check’ function (R package
‘mgcv’) for each tted model (p > 0.90 for all models66).
Received: 31 August 2020; Accepted: 10 December 2020
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We are grateful for the support from Y. Silver, K. Hetterman and S. Linblad, E. Fullerton, M. Saylor, J. and M.
McClurg, For marine operations we thank J. Halvorsen and the crew of the M/Y Marcato, G. Allen, A. Cushwah,
J. Doyle, M. Segren, and S. Rosikov from Fleet Miami, as well as E. Quintero. Additional support was provided
by T. Gilbert and the International Seakeepers Society, J. Todd and P. Nicholson from GIV, and S. Cove. For
logistical and eld assistance we thank S. Kessel, M. Van Zinnicq Bergmann, M. Adunni, J. Pankey, S. Moorhead,
D. Camejo, B. Phillips, S. Teicher, and K. Zacarian. Funding to Beneath the Waves for this work was provided
by a handful of private donors and groups.
Author contributions
O.N.S., C.S.L., N.F., and A.J.G. devised the project concept. O.N.S., E.S., N.H., J.S., S.K., and A.J.G. conducted
eld sampling. C.S.L. and O.N.S. conducted laboratory analysis. O.N.S. and A.J.G. wrote the manuscript with
help from C.S.L., N.F., N.H. All authors approved the nal submission.
Competing interests
e authors declare no competing interests.
Additional information
Supplementary Information e online version contains supplementary material available at https ://doi.
org/10.1038/s4159 8-020-79973 -w.
Correspondence and requests for materials should be addressed to O.N.S.
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... Some pollutants such as mercury, lead, and cadmium have been extensively studied in elasmobranch species (Shipley et al., 2021). However, the majority of the studies are directed at the quantification of these pollutants in different tissues, especially in muscle, the main product derived from fishing for these animals (Barreto et al., 2017;Fowler et al., 2021). ...
... Another problem related to continued exposure to metals is the bioaccumulation of pollutants in organisms. Previous studies indicate that the three species analyzed in this study demonstrate high potential for bioaccumulation (Shipley et al., 2021), with positive correlations observed between the accumulation of metals and the total length of individuals of G. cuvier (Wosnick et al., 2021b). In the present study, the positive relation observed between the length of individuals and the total genomic damage frequency for all sharks, especially N. brevirostris, suggests a bioaccumulation process. ...
... In the present study, the positive relation observed between the length of individuals and the total genomic damage frequency for all sharks, especially N. brevirostris, suggests a bioaccumulation process. This hypothesis is based on the fact that the age of the fish is directly correlated with its length (Trudel and Rasmussen, 1997;Van Walleghem et al., 2007) and because older specimens present slower elimination rates of toxic components and slower growth (Shipley et al., 2021). In this way, these individuals may present an increase in concentrations of metals and other compounds (such as surfactants) in the body, due to the consumption of more contaminated prey over time, as well as an increased time of exposure to environmental contamination (chronic exposure) (Chumchal and Hambright, 2009;Piraino and Taylor, 2009). ...
Elasmobranchs can bioaccumulate and biomagnify pollutants. However, few studies are directed to the effects of pollutants on the health of these animals, and in most cases, are limited to the analysis of biochemical markers. Thus, the incidence of genomic damage among shark species inhabiting a protected ocean island in the South Atlantic was investigated in association with the analysis of pollutants in seawater sample. High levels of genomic damage were identified, especially in Negaprion brevirostris and Galeocerdo cuvier, in addition to interspecific variations that may be related to characteristics such as animal size, metabolism and habits. High concentrations of Surfactants were observed in seawater sample, in addition to low concentrations of Cadmium, Lead, Copper, Chromium, Zinc, Manganese, and Mercury. The results evidenced the potential of shark species as a bioindicator of environmental quality and allowed assessing the anthropic impact on the archipelago, which currently drives its economy through tourism.
... Furthermore, few data on metal accumulation are available for this species. Compared to the scarce worldwide assessments available, Hg concentrations of 0.50 mg kg − 1 in southeastern Brazil (Lacerda et al., 2016), 0.141 mg kg − 1 in northeastern Brazil (Wosnick et al., 2021), 0.42 mg kg − 1 in Florida (Hammerschlag et al., 2016), 0.069 mg kg − 1 in Cuba (Montero-Alvarez et al., 2014), and 9.03 mg kg − 1 in the Bahamas (Shipley et al., 2021) have been reported. To date, Cd and Pb concentrations for nurse sharks are available only for the Bahamian population (0.263 and 0.125 mg kg − 1 , respectively) (Shipley et al., 2021). ...
... Compared to the scarce worldwide assessments available, Hg concentrations of 0.50 mg kg − 1 in southeastern Brazil (Lacerda et al., 2016), 0.141 mg kg − 1 in northeastern Brazil (Wosnick et al., 2021), 0.42 mg kg − 1 in Florida (Hammerschlag et al., 2016), 0.069 mg kg − 1 in Cuba (Montero-Alvarez et al., 2014), and 9.03 mg kg − 1 in the Bahamas (Shipley et al., 2021) have been reported. To date, Cd and Pb concentrations for nurse sharks are available only for the Bahamian population (0.263 and 0.125 mg kg − 1 , respectively) (Shipley et al., 2021). For Rb, our knowledge is even more incipient, with concentrations available only for two arctic species (Pacific sleeper shark, 0.79 mg kg − 1 ; Greenland shark, 0.66 mg kg − 1 ) (McMeans et al., 2007). ...
... In the present study, Hg concentrations reached up to 30.1 mg kg − 1 d.w. (14.2 ± 7.38 mg kg − 1 d.w.; mean ± SD), 3-fold higher than the highest concentration detected for nurse sharks in previous assessments (Shipley et al., 2021). Such data is also interesting when compared with nurse sharks sampled from another region within the BAC (0.141 ± 0.09 mg kg − 1 ; mean ± SD - Wosnick et al., 2021), as Hg concentrations in the nurse sharks from the present study were 106-fold higher. ...
It is widely recognized that apex predators, such as large sharks with highly migratory behavior, are particularly vulnerable to pollution, mainly due to biomagnification processes. However, in highly impacted areas, mesopredator sharks with resident behavior can be as vulnerable as apex sharks. In this context, this study evaluated cadmium (Cd), mercury (Hg), lead (Pb), and rubidium (Rb) concentrations, as well as the potentially protective effects of selenium (Se) and the behavior of two non-enzymatic biomarkers, metallothionein (MT) and reduced glutathione (GSH), employing the Atlantic nurse shark Ginglymostoma cirratum as a study model and compared the results with other resident benthic sharks, as well as highly mobile apex sharks. Muscle tissue samples from 28 nurse sharks opportunistically sampled from the Brazilian Amazon Coast were analyzed. Lower metal concentrations were observed for Pb, Rb and Se in the rainy season, while statistically significant correlations between metals were observed only between Hg and Cd and Pb and Se. Molar ratio calculations indicate potential protective Se effects against Pb, but not against Cd and Hg. No associations between MT and the determined metals were observed, indicating a lack of detoxification processes via the MT detoxification route. The same was noted for GSH, indicating no induction of this primary cellular antioxidant defense. Our results indicate that benthic/mesopredator sharks with resident behavior are, in fact, as impacted as highly mobile apex predators, with the traditional detoxification pathways seemingly inefficient for the investigated species. Moreover, considering the studied population and other literature data, pollution should be listed as a threat to the species in future risk assessments.
... Zafeiraki et al., 2019), and the majority of these were limited to single tissue analyses (e.g. Adams and McMichael, 1999;Storelli et al., 2002;Maz-Courrau et al., 2012;Gilbert et al., 2015;Kim et al., 2016;Matulik et al., 2017;Á lvaro-Berlanga et al., 2021;Shipley et al., 2021). As a consequence, multi-species studies that concurrently investigate the presence of multiple pollutants in more than one tissue are still limited, leaving a gap of knowledge on the species-specific accumulation profile, organotropism, and trophic transfer of pollutants. ...
... Finally, significant correlations between Cd and As were found in both liver and muscle tissues and this may imply that both TEs are introduced into the study area though similar pathways (e.g., upwelling processes; diet, dust deposition, metal-rich particulate/organic matter from runoff or suspended sediments) (Auger et al., 2015;Uren et al., 2020;Shipley et al., 2021). ...
We provided the first multi-species study investigating the presence and organotropism of trace elements in three tissues of 12 elasmobranch species. Shark species showed comparable TE loads, although milk sharks and juvenile scalloped hammerhead sharks exhibited the highest Cd and Hg levels, respectively. Fins accumulated higher levels of Pb, Co, and Cr; muscles higher V, As, and Hg; livers higher Se and Cd levels. The organotropism of TEs calls for cautious when choosing a tissue to be sampled since certain tissues, like fin clips, do not provide reliable surrogate for the internal loads of some TEs. Strong correlations between essential and toxic TEs indicated detoxification mechanisms, while the TMF provided evidence for Hg, As and Se biomagnification along the food-web. Considering the difficulties in assessing elasmobranchs contamination from different areas, the proposed multi-species approach represents a valuable way to estimate the species-specific accumulation and transfer of pollutants in sharks.
... (Berges- Tiznado et al., 2021;García Barcia et al., 2022;Martins et al., 2021;Shipley et al., 2021;Souza-Araujo et al., 2021; data in the ...
Sharks and rays evolved 450 million years ago, during the Late Ordovician Period. However, during the modern Anthropocene, shark populations have declined at considerable rates, and recent global assessments indicate about one in three species is threatened with extinction. A notable reason for this elevated extinction risk is overfishing linked to increased demand for shark fins and other products. Here, we review multiple dimensions of consuming shark products, ranging from stock sustainability, product (mis)labelling and trade, the human health implications of consuming shark products, and illegal, unreported and unregulated fishing and slavery and labour abuses in the fishing industry. We conclude that traceability and increased transparency in seafood supply chains is essential to overcome obstacles to consumption of sustainable, ethical and healthy shark products. We also provide a decision tree outlining steps in consumer choice that would foster such consumption. Our aim is to provide a holistic view on issues concerning the consumption of shark products that will help policymakers, the public, management and law enforcement agencies to advocate for ecologically‐ and ethically sustainable consumption of shark products and thereby empower the general public to make informed decisions on which shark products they consume.
... In this study, linear regression analysis did not reveal a significant relationship between shark length/weight and metal concentration in each species. However, length/metals or weight/metals relationships have been reported in the previous study [5,46]. We observed a significant relationship between habitat (coastal/pelagic sharks vs. deep-water/benthic sharks) and metal concentration. ...
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Metals accumulation in threatened sharks’ meat represents a global health issue. The objective of the current study was to measure the concentration of six metals (Li, Ti, Ni, Cd, As, and Pb) using ICP-MS in threatened sharks’ meat of Rhizoprionodon acutus, Squalus hemipinnis, and Sphyrna lewini from Binuangeun Fish Auction in Lebak, Banten, Indonesia. The results showed that the concentration of Ni, Li, Cd, and Pb was below the acceptable levels for food sources for human consumption, except for As concentration (more than 30 fold higher). This study showed high levels of Ti concentration in all threatened sharks' meat. Overall, this study shows that an accumulation of Ti in sharks' meat should be considered a risk to the health of seafood consumers.
... Over the last century, rapid industrialization and urbanization processes have pointedly increased the accumulation of toxic elements in large-bodied predators (e.g., sharks) causing delayed growth, reproductive damages, and greater prevalence of diseases in organisms, which may also result in neurotoxicological/carcinogenic impacts for public health, when the organisms are used as a food source for human consumption (Shipley et al., 2021). Nevertheless, biodilution/biomagnification processes in a food web structure are essential to understand the vulnerability of a marine system. ...
Stable isotopic values of carbon (δ¹³C) and nitrogen (δ¹⁵N) were used to characterize the trophic structure and biomagnification of Cadmium (Cd), Mercury (Hg) and Selenium (Se) in a trophic web of 18 taxa namely zooplankton, crustaceans, mollusks, fishes, and Mustelus henlei shark collected off the western coast of Baja California Sur, Mexico. Isotopic results indicated interspecies variations in the trophic web structure with mean δ ¹³C values of – 20.0 ‰ (zooplankton) < − 18.2 ‰ (M. henlei) < − 14.1 ‰ (Thaisella kiosquiformis, mollusk). In general, δ¹⁵N and δ¹³C values increased from primary consumers (zooplankton) to predators, following the isotopic patterns of other trophic webs. The concentrations of Cd, Hg and Se were relatively less in most of the organisms except mollusks that presented high concentrations of Cd. The biomagnification factors of the trophic web showed biodilution of Cd (Food Web Magnification Factor, FWMFCd = 0.2), biomagnification of Hg (FWMFHg = 3.34) and Se (FWMFSe = 1.45) respectively. However, the concentrations of Se did not increase consistently from the lower trophic levels to the higher ones. This study documents the dynamics of a marine trophic structure and demonstrates that biodilution/biomagnification processes of metal contaminants are largely species specific and are closely related to physical - chemical and food web structure.
... and Cedeño-Macias, 2016; Di Bella et al., 2020) and bony fish (Barone et al., 2021;Vetsis et al., 2021;Storelli et al., 2022). The biomagnification of trace elements can be affected by several factors (Boldrocchi et al., 2021) like the species ecology (Shipley et al., 2021), their diet and trophic level (Medina-Morales et al., 2020;Vetsis et al., 2021), the trophic web complexity (Wang, 2002) and the human activities in an area (Adel et al., 2018). In our work we detected similar levels for most trace elements with the relevant global bibliography (Tiktak et al., 2020) and the relevant Greek and Mediterranean studies (Kousteni et al., 2006;Storelli et al., 2010;Mille et al., 2018;Vetsis et al., 2021). ...
Trace elements have the potential to bioaccumulate in marine organisms and to biomagnify towards the upper levels of marine trophic webs, resulting in a range of negative effects on organisms. Elasmobranchs are highly susceptible to bioaccumulation of trace metals, while their consumption by humans is increasing worldwide. Therefore, it is important to monitor the trace metal content in the edible tissues of elasmobranchs. This work reveals the content of 12 trace metals in the edible tissues of 10 elasmobranch species caught in Greek waters. Levels above the permissible limits for Hg and Pb were found in some species, while analysis of the lifetime consumption risk for adults and children using the Target Hazard Quotient (THQ), revealed a high risk for two of the most toxic substances on the priority list for substances, namely As and Hg. These are preliminary results, and further research is required to understand better the issue.
... Among the variety of pollutants found in the marine environment, heavy metals are frequently assessed owing to their high persistence, toxicity, and bioaccumulative affinities (Naser, 2013;Wang et al., 2013). In the marine environment, Mercury (Hg) is ubiquitously present in elasmobranchs and is increasingly being reported worldwide (Pantoja-Echevarría et al., 2020;Reistad et al., 2020;Shipley et al., 2021;Murillo-Cisneros et al., 2021;Endo et al., 2021). This is mainly caused by bioaccumulation and biomagnification (Wang et al., 2013;McMeans et al., 2015). ...
A study on mercury (Hg) and selenium (Se) concentrations in the liver and muscle of brown smooth-hound shark Mustelus henlei and its principal prey items, was conducted in the western coast of Baja California Sur, Mexico. Average Hg concentrations were found to be high in the muscle than in the liver; however, Hg concentrations were below the maximum permissible limits, and hence, the consumption of this species does not constitute a risk to human health. The mean Se concentrations were higher in the liver than in the muscle. The results of Hg: Se molar ratio revealed that Se counteracts the toxicity of Hg in hepatic tissues, whereas the contrary occurs in the muscle. Significant differences in Hg and Se accumulation were observed between females and males. Biomagnification factor values >1 demonstrate a biomagnification process from its principal prey species (i.e., red crab, Pleuroncodes planipes and Pacific mackerel, Scomber japonicus).
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Blue sharks (Prionace glauca) are an important resource in Ecuador’s fisheries; however, biological and ecological information of this species in the area is scarce. The goal of this study was to determine Hg and Cd concentration levels in muscle tissue, as well as its relationship with size, sex, and sexual maturity stages. A total of 80 specimens (34 females and 46 males) collected from the Ecuadorian longline fishing fleet between June and December 2012 were examined. Sizes for females ranged from 97 to 280 cm total length, with values of Hg between 0.20 to 2.38 mg kg⁻¹ wet weight (x̄ = 0.71, ± 0.61) and values of Cd between 0.01 and 0.12 mg kg⁻¹ (x̄ = 0.04, ± 0.02). Sizes for males ranged from 137 to 290 cm TL with values of Hg between 0.17 and 2.94 mg kg⁻¹ (x̄ = 0.81, ± 0.68) and Cd concentrations between 0.01 and 0.12 mg kg⁻¹ (x̄ = 0.04, ± 0.03). A Spearman’s rank correlation showed a medium positive association between TL and Hg concentrations (ρ = 0.66; p < 0.05), but there was no correlation between TL and Cd concentrations (ρ = 0.00, p < 0.05). Of the analyzed sharks, 46% and 20% had Hg and Cd concentrations, respectively, greater than the limit established by authorities for fishes consumed by humans.
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The rapid expansion of human activities threatens ocean-wide biodiversity. Numerous marine animal populations have declined, yet it remains unclear whether these trends are symptomatic of a chronic accumulation of global marine extinction risk. We present the first systematic analysis of threat for a globally distributed lineage of 1,041 chondrichthyan fishes-sharks, rays, and chimaeras. We estimate that one-quarter are threatened according to IUCN Red List criteria due to overfishing (targeted and incidental). Large-bodied, shallow-water species are at greatest risk and five out of the seven most threatened families are rays. Overall chondrichthyan extinction risk is substantially higher than for most other vertebrates, and only one-third of species are considered safe. Population depletion has occurred throughout the world's ice-free waters, but is particularly prevalent in the Indo-Pacific Biodiversity Triangle and Mediterranean Sea. Improved management of fisheries and trade is urgently needed to avoid extinctions and promote population recovery.
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The oceanic whitetip shark Carcharhinus longimanus is a widely distributed large pelagic shark species once considered abundant in tropical and warm temperate waters, but recently listed as Critically Endangered by the IUCN due to drastic population declines associated with overfishing. In addition to risks posed to its populations due to overexploitation, oceanic whitetip sharks are also capable of accumulating elevated quantities of harmful environmental toxicants, placing them at special risk from anthropogenic pollution. Herein, we provide the first data on accumulation of the toxic, non-essential metal mercury (Hg) in northwest Atlantic (NWA) oceanic whitetip sharks, focusing on aggregations occurring at Cat Island, The Bahamas. Total Hg (THg) concentrations were measured in muscle of 26 oceanic whitetip sharks and compared with animal length and muscle δ ¹⁵ N to evaluate potential drivers of Hg accumulation. THg concentrations were also measured in fin and blood subcomponents (red blood cells and plasma) to determine their value as surrogates for assessing Hg burden. Muscle THg concentrations were among the highest ever reported for a shark species and correlated significantly with animal length, but not muscle δ ¹⁵ N. Fin, red blood cell, and plasma THg concentrations were significantly correlated with muscle THg. Fin THg content was best suited for use as a surrogate for estimating internal Hg burden because of its strong relationship with muscle THg levels, whereas blood THg levels may be better suited for characterizing recent Hg exposure. We conclude that Hg poses health risks to NWA oceanic whitetip sharks and human consumers of this species.
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Stable isotopes have provided important insight into the trophic structure and interaction in many ecosystems, but to date have scarcely been applied to the complex food webs of coral reefs. We sampled white muscle tissues from the fish species composing 80% of the biomass in the 4–512 g body mass range at Cape Eleuthera (the Bahamas) in order to examine isotopic niches characterised by δ¹³C and δ¹⁵N data and explore whether fish body size is a driver of trophic position based on δ¹⁵N. We found the planktivore isotopic niche was distinct from those of the other trophic guilds suggesting the unique isotopic baseline of pelagic production sources. Other trophic guilds showed some level of overlap among them especially in the δ¹³C value which is attributable to source omnivory. Surprising features of the isotopic niches included the benthivore Halichoeres pictus, herbivores Acanthurus coeruleus and Coryphopterus personatus and omnivore Thalassoma bifasciatum being close to the planktivore guild, while the piscivore Aulostomus maculatus came within the omnivore and herbivore ellipses. These characterisations contradicted the simple trophic categories normally assigned to these species. δ¹⁵N tended to increase with body mass in most species, and at community level, the linear δ¹⁵N–log2 body mass relationship pointing to a mean predator–prey mass ratio of 1047:1 and a relatively long food chain compared with studies in other aquatic systems. This first demonstration of a positive δ¹⁵N–body mass relationship in a coral reef fish community suggested that the Cape Eleuthera coral reef food web was likely supported by one main pathway and bigger reef fishes tended to feed at higher trophic position. Such finding is similar to other marine ecosystems (e.g. North Sea).
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Shark meat is consumed as a food source worldwide, especially in Asian countries. However, since sharks are apex predators in the ocean food chain, they are prone to bioaccumulation of heavy metals. More than 100 million sharks are caught annually for human consumption, and the safety of shark meat cannot be overemphasized. Here, we examined heavy metal concentration in the muscle tissue of 6 shark species including 3 migratory species (Carcharhinus brachyurus, Carcharhinus obscurus, and Isurus oxyrinchus) and 3 local species (Triakis scyllium, Mustelus manazo, and Cephaloscyllium umbratile) from fish markets in Jeju Island, Republic of Korea. The concentrations of 11 heavy metals (Cr, Fe, Cu, Zn, As, Se, Cd, Sn, Sb, Pb, and Hg) and MeHg were analyzed. The result showed that the average concentrations of all metals, except for that of As, were below the regulatory maximum limits of many organizations, including the Codex standard. Hg and MeHg were significantly correlated with body length, body weight, and age, and the concentration of Hg was expected to exceed the limit in C. brachyurus with a body length or weight of over 130 cm or 25 kg, respectively. Our results indicate that shark meat can expose consumers to a high level of As and that copper sharks bigger than the predicted size should be avoided for excessive Hg. Considering these findings, a detailed guideline on consumption of meat of different shark species should be suggested based on further investigation. © 2019 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
This review represents a comprehensive analysis on pollutants in elasmobranchs including meta-analysis on the most studied pollutants: mercury, cadmium, PCBs and DDTs, in muscle and liver tissue. Elasmobranchs are particularly vulnerable to pollutant exposure which may pose a risk to the organism as well as humans that consume elasmobranch products. The highest concentrations of pollutants were found in sharks occupying top trophic levels (Carcharhiniformes and Lamniformes). A human health risk assessment identified that children and adults consuming shark once a week are exposed to over three times more mercury than is recommended by the US EPA. This poses a risk to local fishing communities and international consumers of shark-based products, as well as those subject to the widespread mislabelling of elasmobranch products. Wider screening studies are recommended to determine the risk to elasmobranchs from emerging pollutants and more robust studies are recommended to assess the risks to human health.
Factors influencing organic contaminant accumulation in sharks, especially across ontogeny, are not well known. Contaminant concentrations were measured in three species of sharks (Blue, Shortfin Mako and Common Thresher) across a range of size classes (neonatal to adult) that vary in their ecological and physiological characteristics. Empirical data was compared to a theoretical framework that predicted the shape of lifetime accumulation curves. We found that a one-size-fits-all accumulation model was not appropriate as species-specific characteristics had a significant effect on contaminant accumulation trajectories. Maternal offloading likely has an important effect on determining neonatal shark contaminant starting points, and trophic ecology and physiology may interact to affect the shape of species’ contaminant accumulation curves. Makos were found to have the highest accumulation potential and Blues the lowest, with Threshers intermediate. Changes in species’ ecology and/or physiology were also reflected in contaminant signature changes over ontogeny. If contaminant concentrations are to be used as a proxy for risk, species-specific characteristics need to be taken into account when estimating contaminant exposure and its potential negative effects on shark health and human consumption safety.
Observations of resource use dynamics are sparse for higher trophic level species in marine systems, but important given their role in driving the distribution and functional roles of species. For a guild comprised of seven large-bodied shark species captured in Florida Bay, we use multi-tissue stable isotope analysis to evaluate the extent of resource use diversity within and between two time periods. We examine: 1) variation in community-wide isotopic niche structure across time (i.e., Layman’s community metrics); 2) variation in species’ trophic position (TP); 3) reliance upon dominant resource pools (inland mangroves vs. coastal neritic [i.e. seagrass and/or reef-associated prey]; and 4) patterns of intraspecific isotopic variation across species (i.e., standard ellipse area [SEAc], ellipse eccentricity [E], ellipse inclination [θ], and total isotopic overlap). Community-wide isotopic niche characteristics varied with tissue type, suggesting temporal plasticity in community resource use. Our novel approach integrating multiple isotopic baselines resulted in consistently high trophic position estimates (> 5.0), but the utilization of available resource subsidies varied with species and tissue type. Whole blood suggested recent use of inland mangrove-derived prey resources while fin tissue suggested differential use of both inland mangroves and coastal neritic-derived subsidies. Our results suggest that sharks display dynamic resource use in space and time, with limited functional complementarity across species. The adoption of diverse resource use strategies, both within and among species, could facilitate the co-occurrence of large-bodied predator species and underscores the role of sharks as vectors of ecosystem connectivity.