Bioaccumulation of Metals in Tissues of Seahorses Collected from Coastal China

Abstract

Seahorses, which have been used in Chinese traditional medicine, are poor swimmers and easily affected by regional ecological conditions. In this study, we investigated the bioaccumulation of nine metals in different tissues of four seahorse species (Hippocampus trimaculatus, H. histrix, H. kelloggi, and H. kuda) from six locations along the Chinese coast. The present study found relatively low concentrations of metals in the seahorses compared with those in other marine fishes. There was a location-dependent variation in metal concentrations in the seahorses, especially between developed and less developed cities. Results also showed metal concentrations varied among different seahorse species and tissues, with H. kelloggi having higher bioaccumulation ability compared with H. trimaculatus and higher metal levels were found in visceral mass, muscle, and skin tissues than those in brain, lips gill, endoskeleton, and exoskeleton tissues in the seahorses. Among different metals, Mg had the highest tissue concentrations in all the seahorses, followed by Al and Mn.

Full text

Bioaccumulation of Metals in Tissues of Seahorses Collected
from Coastal China
Wei Zhang
1
•Yanhong Zhang
1
•Li Zhang
1
•Qiang Lin
1
Received: 12 June 2015 / Accepted: 5 January 2016
ÓSpringer Science+Business Media New York 2016
Abstract Seahorses, which have been used in Chinese
traditional medicine, are poor swimmers and easily affec-
ted by regional ecological conditions. In this study, we
investigated the bioaccumulation of nine metals in different
tissues of four seahorse species (Hippocampus trimacula-
tus,H. histrix,H. kelloggi, and H. kuda) from six locations
along the Chinese coast. The present study found relatively
low concentrations of metals in the seahorses compared
with those in other marine fishes. There was a location-
dependent variation in metal concentrations in the sea-
horses, especially between developed and less developed
cities. Results also showed metal concentrations varied
among different seahorse species and tissues, with H. kel-
loggi having higher bioaccumulation ability compared with
H. trimaculatus and higher metal levels were found in
visceral mass, muscle, and skin tissues than those in brain,
lips gill, endoskeleton, and exoskeleton tissues in the sea-
horses. Among different metals, Mg had the highest tissue
concentrations in all the seahorses, followed by Al and Mn.
Keywords Metals Bioaccumulation Tissue Seahorse
A recent report indicated that industrial and domestic
sewage discharges, mining, smelting, and electronic waste
recycling are important sources for metal pollution in
estuarine and coastal Chinese waters (Pan and Wang 2012).
The sources of the metals are highly variable and
complicated due to the variation of regions and human
activities (Lewis et al. 2002; Kojadinovic et al. 2007). Most
importantly, toxic metals are persistent and can be accu-
mulated in organisms and be transferred to human via food
chain and cause potential health risk (Pourang and Dennis
2005). Seahorses are a group of marine fishes used in
Chinese traditional medicines, thus, the investigation of
metal concentrations in their tissues is important for
understanding the potential human health risks associated
with such use.
Seahorses belong to the genus Hippocampus and are
widely distributed in tropical shallow sea and are vulner-
able to habitat destruction (Lourie et al. 1999). In recent
years, the seahorse resources have been greatly affected by
the over-exploitation to meet the heavy demands from
Chinese traditional medicine industry, ornamental and
curio markets (Martin-Smith et al. 2004; Lin et al. 2009,
2012). Therefore, seahorses have been listed in Appendix II
of the Convention on International Trade in Endangered
Species of Wild Fauna and Flora (IUCN 2011). Water
quality and human mediated anthropogenic activities are
among the most important factors affecting seahorse con-
servation (Lourie et al. 1999; Foster and Vincent 2004).
Unlike most other fishes, seahorses are poor swimmers and
have small home ranges during their life history (Qin et al.
2014), so they are easily affected by the regional water
conditions. In comparison with other factors for fish spe-
cies, the behavior and physiological characteristics also
play essential roles in the metal accumulations from the
water (Burger and Gochfeld 2005).
The present study aimed to investigate the bioaccumu-
lation of metals in wild seahorses from the Chinese coast
(from the high to low latitudes). Different locations were
used to evaluate the effect of enviromental conditions on
metal accumulation in the seahorses. Different seahorse
&Qiang Lin
linqiangzsu@163.com
1
CAS Key Laboratory of Tropical Marine Bio-resources and
Ecology, Guangdong Provincial Key Laboratory of Applied
Marine Biology, South China Sea Institute of Oceanology,
Chinese Academy of Sciences, Guangzhou 510301,
People’s Republic of China
123
Bull Environ Contam Toxicol
DOI 10.1007/s00128-016-1728-4

species and tissues were used to test whether there were
any interspecific or tissue variations in the seahorses. The
overall results will help improve our knowledge on metal
accumulation in the seahorses from coastal China.
Materials and Methods
With the help of the local fishermen, a total of four species of
seahorses were obtained from six locations along the Chi-
nese coast between October and November 2010, including
Qingdao, Zhoushan, Xiamen, Shanwei, Zhanjiang, and
Beihai (Fig. 1). The samples of Hippocampus trimaculatus,
H. histrix,H. kelloggi, and H. kuda were approximately
14.7 ±2.15 (14–16) cm, 13.9 ±1.76 (13–15) cm,
18.7 ±2.08 (17–20) cm, and 15.1 ±1.34 (14–16) cm in
standard body length, respectively. For each species, nine
replicates (comprised of three individuals) were sampled for
the analysis. After transferring the samples to the laboratory,
different tissues of the seahorses were dissected apart using a
pre-cleaned stainless steel instruments. Exoskeletons were
first rinsed with acetone solution to remove the epibionts, and
rinsed three times in Mill-Q water (Millipore 18.2 M). Then
different tissues were dried at 105°C until constant weight,
after which they were ground to fine powder in a mortar and
pestle. The dry weights were recorded, and then the samples
were stored at room temperature until analysis. All seahorses
used for this study were collected following the appropri-
ate animal ethics guidelines as approved by the Chinese
Academy of Sciences.
The digestion of seahorse tissues were carried out using
a microwave assisted digestion. Exact 0.5 g of dry samples
were transferred to a digestion vessel, and added with 5 mL
aqua regia (HNO
3
: HCl =1: 3). Typically, the tempera-
ture was ramped slowly to 190°C without over pressur-
ization and held at 190°C for 10 min. After the samples
cooled and the dissolved gases were dissipated, digested
samples were transferred into a 25 mL volumetric flask,
and then added Mill-Q water to a volume of 25 mL. The
digests were then diluted with Mill-Q water for metals
analysis. A blank digest was carried out in the same way.
The samples were analyzed for Al, Ba, Cd, Ce, Cr, Cu, Mg,
Mn, and Pb, using inductively coupled plasma mass
spectrometer (ICP-MS). The standard solution was pre-
pared from a stock solution (National Analysis Center for
Iron and Steel, China).
The accuracy of our digestion method was verified by
analysis of standard reference material (SRM) of 2976
mussel tissue (National Institute of Standards and Tech-
nology, the National Research Council Canada, and the
International Atomic Energy Agency, Marine Environment
Laboratory, Monaco). Limits of detection (LOD) were
defined as three times the signal-to-noise ratio for the
analyzed matrix or blank value for each sample. The
method detection limit (MDL) was defined either as three
times the standard deviation of the blank samples or, if the
blanks had no detectable contamination, as the instru-
mental detection limit (IDL). IDL values were all lower
than 0.1 ng/L. Based on our digestion and dilution meth-
ods, the LOD value of each tissue was 0.005 ng/g. The
Fig. 1 Sampling locations
along the Chinese coast
(Qingdao, Zhoushan, Xiamen,
Shanwei, Zhanjiang, Beihai)
and the metal composition (Al,
Ba, Cd, Ce, Cr, Cu, Mg, Mn,
and Pb) in seahorse samples
(Hippocampus trimaculatus,
H. kuda, H. histrix, and
H. kelloggi)
Bull Environ Contam Toxicol
123

recovery rate was Al 86.4 %, Cd 100.2 %, Ce 98.2 %, Cr
101.2 %, Cu 99.2 %, Mg 96.1 %, Mn 99.2 %, and Pb
89.9 %, respectively. During the test, there was no Ba
standard reference, so the recovery rate of Ba was not
determined. Concentrations of Al and Mg were expressed
as lg/g dry weight, and those of Ba, Cd, Ce, Cr, Cu, Mn,
and Pb were expressed as ng/g dry weight.
Statistical analyses were performed using SPSS version
16.0. The differences of the corresponding values between
the control and exposed groups were tested by one-way
analysis of variance (ANOVA) followed by a Duncan test
where normality and homogeneity were met. A probability
level (pvalue) of \0.05 was regarded as statistically
significant.
Results and Discussion
H. trimaculatus was used as the representative seahorse to
study the relationship between the metal concentrations
and the geographic areas because this species has a wide
distribution along the Chinese coast (Zhang et al. 2014).
The concentrations of nine metals in the visceral mass of
H. trimaculatus are shown in Fig. 1and Fig. 2.
The ranges of metal concentrations of Al, Ba, Cd, Ce,
Cr, Cu, Mg, Mn, and Pb in H. trimaculatus were
0.05–0.43 lg/g, 5.99–37.5 ng/g, 1.26–4.52 ng/g, 0.61–4.93
ng/g, 4.3–46.3 ng/g, 3.91–17.0 ng/g, 0.82–2.25 lg/g,
18.0–88.8 ng/g, and 10.1–33.6 ng/g among all the loca-
tions (Fig. 1). Seahorses had the highest concentrations of
Al (0.43 lg/g), Ce (4.93 ng/g), Cu (17.0 ng/g), Mn
(88.8 ng/g), and Pb (33.6 ng/g) at Qingdao, and the highest
concentrations of Ba (37.5 ng/g), Cd (4.52 ng/g), and Cr
(46.3 ng/g) occurred in seahorses at Xiamen. Seahorses at
Zhoushan had the highest Mg concentration (2.25 lg/g).
Furthermore, the highest concentrations of Al, Cd, Cu, and
Mn were found at both Qingdao and Xiamen. The lowest
concentrations of Al (0.05 lg/g), Ba (5.99 ng/g), Ce
(0.61 ng/g), and Mn (18.0 ng/g) in seahorses were found at
Zhoushan, and the lowest concentrations of Cd (1.26 ng/g),
Cu (3.91 ng/g), Mg (0.82 lg/g), and Pb (10.1 ng/g) in
seahorses were found at Beihai. Interestingly, the concen-
trations of Cr in seahorses varied 10.8 times between
Xiamen and Zhanjiang, which indicates that there is a
considerable difference in the bioavailability of this metal.
In the present study, the results showed the higher metal
levels in seahorses at Qingdao and Xiamen, and concen-
trations of metals in H. trimaculatus showed a location-
dependent variation.
In this finding, the metal concentrations in seahorses
may reflect the intensities of industrial activity in these
regions. Qingdao and Xiamen exhibited the fastest
Concentration (µg/g)
0.0
0.2
0.4
0.6
Al
Concentration (ng/g)
0
15
30
45 Ba
Concentration (ng/g)
0
2
4
6
8Cd
Concentration (ng/g)
0
2
4
6Ce
Concentration (ng/g)
0
20
40
60 Cr
Concentration (ng/g)
0
5
10
15
20 Cu
Qingdao
Zhoushan
Xiamen
Zhanjiang
Beihai
Concentration (µg/g)
0
1
2
3Mg
Qingdao
Zhoushan
Xiamen
Zhanjiang
Beihai
Concentration (ng/g)
0
40
80
120 Mn
Qingdao
Zhoushan
Xiamen
Zhanjiang
Beihai
Concentration (ng/g)
0
20
40
60 Pb
d
a
c
bb
b
aa
cc
c
b
c
b
a
d
a
c
ab
bc b
bc
d
a
c
d
b
c
b
a
de
b
c
a
d
a
c
bb
bb
a
aa
Fig. 2 Different metal concentrations in the visceral mass of the seahorse H. trimaculatus from different locations. Data are mean ±SD.
Different letters represent significant differences among different locations (p\0.05)
Bull Environ Contam Toxicol
123

economic development over the past two decades. In ear-
lier studies, the metal contamination in surface sediments
of the Jiaozhou Bay, Qingdao, showed significant vari-
ability and ranged from 4.2 to 28 mg/kg for Cu, 5.2 to
18 mg/kg for Pb, 0.03 to 0.11 mg/kg for Cd (Wang et al.
2007). Xiamen Bay (XMB) had received substantial load-
ings of pollutants from industrial and municipal wastewater
discharge since the 1980s. The metal concentrations in
sediments of the Jiulongjiang River were as follows, Pb:
42–55 mg/kg; Cr: 28–29 mg/kg; Cd: 175–423 mg/kg (Yan
et al. 2010). Therefore, the sediments of the Qingdao and
Xiamen have been contaminated by metals to different
degrees. Notably, seahorses are small carnivorous demersal
fish and have small home ranges (Vincent et al. 2011), thus,
high metal concentrations in seahorses may be attributed to
high metal concentrations in the sediments of Qingdao and
Xiamen. Moreover, among the five locations, the lowest
concentrations of Al, Ba, Ce, and Mn in H. trimaculatus
were found at Zhoushan, and the lowest concentrations of
Cd, Cu, Mg, and Pb were found at Beihai. Such results
were consistent with the fact that Zhoushan and Beihai
were tourist island cities with less industrial activities. The
atmospheric deposition (automobile emissions and indus-
trial discharges) in Beihai was taken into account in the
assessment because atmospheric deposition is one of the
principal pathways of transport for anthropogenic Cd and
Pb. Since there were relatively few automobiles and
industries, the Cd and Pb concentrations in seahorses from
Beihai were the lowest among all the locations. In the
present study, Cr levels in seahorses collected from Xia-
men was 10.8 times higher than those from Zhanjiang,
which seemed to suggest a dependency on an external
source of Cr. This can also be ascribed to more industrial
activities in Xiamen. In other words, Xiamen has been
seriously contaminated with Cr. Zhang et al. (2007)
reported that the surface sediments collected from the
western Xiamen Bay, were moderately polluted by Cr,
where sewage outlets and commercial ports were the main
sources of contaminants to the area.
Cd levels in seahorses ranged from 0.60 to 107.3 ng/g,
and the highest Cd concentration (107.3 ng/g) was found in
the muscle tissue of H. kelloggi at Zhanjiang. Moreover,
Cd levels in seahorses were lower than those in other
marine fish (1–400 ng/g) (Zheng et al. 2007; Tepe et al.
2008; Zhang and Wang 2012). Similarly, Cr levels in
seahorses were 2.67–49.3 ng/g. In comparison, Cr levels in
marine fish from the Pearl River Estuary have been mea-
sured as 110–4270 ng/g ww, 40–220 ng/g ww,
17.6–121 ng/g dw (Ip et al. 2005; Cheung et al. 2008;
Zhang and Wang 2012). Thus, the Cr levels in seahorses
were lower than those in marine fish from the Pearl River
Estuary. Cu levels in seahorses were 3.91–41.4 ng/g. In
previous studies, Cu concentrations in marine fish were
generally found to be within the range of 0.4–7.8, 0.51–7.0,
and 0.34–7.35 lg/g dw (Tu
¨rkmen et al. 2009; Onsanit et al.
2010; Zhang and Wang 2012). Interestingly, seahorses had
low assimilation and bioavailability for Cu in aquatic
environment. Therefore, the bioaccumulation kinetics of
Cu in seahorses needs to be explored in the future. Mn and
Pb concentrations in seahorses (18.0–261.4 and
7.44–126.6 ng/g) were also low when compared with those
in other marine fish (Uluozlu et al. 2007; Tepe et al. 2008;
Tu
¨rkmen et al. 2009). Seahorses swim slowly within the
coral, seagrass, and mangrove habitats in temperate and
tropical ocean regions (Lourie et al. 1999; Teske and
Beheregaray 2009), and they have poor swimming ability
in comparison with other marine fish (Ashley-Ross 2002).
Furthermore, the poor swimming seahorses may have
lower feeding frequency than other marine fish with good
swimming capabilities (Qin et al. 2012), and their digestive
systems are simple and not very efficient in terms of
absorption (Michael 2001). These special behaviors of the
seahorses may partly explain their relatively low metal
concentrations. Thus, the limited bioaccumulation ability
in seahorses may be attributed to their behaviors and other
factors, which will be worth investigating in the future.
Of the 9 metals quantified, Mg had the highest tissue
concentrations in the seahorses, followed by Al, Mn, Pb,
Ba, Cr, Cu, Cd, and Ce. The sequences of metal concen-
trations varied among different seahorse species and loca-
tions. The concentrations of metals in the studied seahorses
clearly revealed that seahorses were differentially selective
for a range of metals. Among all the locations, four sea-
horse species all showed high levels of Mg, Al, and Mn
(Table 2). In Xiamen, the mean concentrations of Al, Ba,
Cd, Ce, Cu, Mg, and Mn in H. trimaculatus and H. histrix
were comparable. Only Cr and Pb concentrations in H.
trimaculatus were significantly higher than those in H.
histrix (Table 1). These results indicate that the bioaccu-
mulation of metals in H. trimaculatus and H. histrix were
comparable, which might be due to the trophic transfer
from their prey, such as invertebrates. In Zhanjiang, the Al,
Ba, Cd, Ce, Cr, Cu, and Pb concentrations in H. kelloggi
were significantly higher than those in H. trimaculatus,
while the Mg and Mn concentrations in H. trimaculatus
were significantly higher than those in H. Kelloggi
(Table 1). Therefore, H. kelloggi showed higher bioaccu-
mulation ability compared with H. trimaculatus. Such
differences may be caused by different biokinetics of
metals. Zhang and Wang (2012) reported that the trace
metal levels varied significantly with species, such differ-
ences of metal accumulation in marine fish may be due to
their different biokinetics. Rainbow (2002) also reported
that biodynamics captured the biologically driven patterns
that differentiated bioaccumulation among species. On the
other hand, such interspecific differences may be due to
Bull Environ Contam Toxicol
123

feeding ecology (Foster and Vincent 2004; Burger and
Gochfeld 2005). Most of previous studies affirmed that
seahorses were likely to attach themselves to substrates
(fixed or floating) (Caldwell and Vincent 2013; Luzzatto
et al. 2013). H. trimaculatu was reported to mainly inhabit
among gorgonians at approximately 20–40 m depth,
whereas H. kelloggi inhabited gorgonians and sea whips in
deep-water below 65 m throughout the coastal waters of
the Peninsular and East Malaysia (Choo and Liew 2003;
Kuang and Chark 2004). Thus, H. kelloggi lived in lower
water layer compared with H. trimaculatus. Coincidentally,
we observed relatively high levels of metals in H. kelloggi,
which strongly demonstrates that ingestion of benthic preys
may contribute to such high levels of metals in H. kelloggi.
Therefore, metal concentrations varied among different
seahorses, which were similar with other marine fishes.
Previous studies have reported that metals concentrations
in fish muscles varied widely among different fish species
(Zhang and Wang 2012). Falco
´et al. (2006) also suggested
that different concentrations of As, Cd, Hg, Mn, Pb, and Se
in fish were found in New Jersey and Catalonia, and con-
cluded that there were significant interspecific differences
for all metals.
The concentrations of nine metals in different tissues
of collected seahorses are shown in Table 2. For H. tri-
maculatus from Qingdao, Al, Ce, Cr, and Pb levels in
visceral mass, and Ba, Cd, Ce, Cu levels in endoskeleton
were significantly higher than those in other tissues
(p\0.05). In comparison, H. trimaculatus from
Zhoushan loaded significantly higher Al, Cu, and Mn
concentrations in lips gill than those in brain, visceral
mass, and muscle. In Xiamen, Ba, Cd, Ce, Cr, and Cu
levels in visceral mass of H. trimaculatus were signifi-
cantly higher than those in other tissues (p\0.05).
However, Al, Mg, and Mn in brain of H. histrix were
significantly higher than those in other tissues (p\0.05).
In Shanwei, Cr, Cu, and Mg levels in visceral mass and
skin of H. kuda were significantly higher than those in the
exoskeleton and muscle (p\0.05). In Zhanjiang, Al, Cd,
Ce, Cu, Mn, and Pb levels in muscle of H. trimaculatus
were significantly higher than those in other tissues
(p\0.05). Al, Ba, Ce, and Cu levels in skin and Cd, Ce,
and Cu levels in muscle were significantly higher than
those in other tissues in H. kelloggi (p\0.05). In Beihai,
Cr concentrations in brain, lips gill, and visceral mass
were significantly higher than those in other tissues in H.
trimaculatus (p\0.05). Thus, metal concentrations in
different tissues of the seahorses from different locations
varied dramatically.
The metals were mainly distributed in visceral mass,
muscle, and skin of seahorses. Earlier studies found high
metal concentrations in visceral mass, which may be due to
direct contact with the food and seawater in the gut or the
Table 1 Metal concentrations (dry weight basis) in seahorse species from different locations of the Chinese coast
Locations Species Metal concentrations
Al (lg/g) Ba (ng/g) Cd (ng/g) Ce (ng/g) Cr (ng/g) Cu (ng/g) Mg (lg/g) Mn (ng/g) Pb (ng/g)
Xiamen H. trimaculatus 0.95 ±0.06
a
141.4 ±17.0
a
18.2 ±5.10
a
9.35 ±0.39
a
130.9 ±57.1
b
59.7 ±14.8
a
9.40 ±1.14
a
445.8 ±46.3
a
214.3 ±18.5
b
H. histrix 0.90 ±0.04
a
120.3 ±11.8
a
15.6 ±0.04
a
9.67 ±0.74
a
121.3 ±14.9
a
58.5 ±12.6
a
11.7 ±0.65
a
412.3 ±69.1
a
115.7 ±18.7
a
Zhanjiang H. trimaculatus 1.11 ±0.05
a
114.2 ±9.99
a
23.6 ±1.15
a
11.3 ±0.20
a
55.1 ±0.22
a
63.3 ±0.91
a
10.3 ±0.73
b
555.4 ±47.9
b
134.3 ±6.75
a
H. kelloggi 1.62 ±0.40
b
167.6 ±12.3
b
132.1 ±8.51
b
14.9 ±0.53
b
56.3 ±1.87
b
73.1 ±7.82
b
8.51 ±2.11
a
763.0 ±29.7
a
144.2 ±22.2
b
Data are mean ±SD (n =9). For each metal, different letters indicate significant differences among seahorse species in the same location
Bull Environ Contam Toxicol
123

Table 2 Metal concentrations (dry weight basis) in seahorse species from different locations of the Chinese coast
Locations Species Tissues Metal concentrations
Al (lg/g) Ba (ng/g) Cd (ng/g) Ce (ng/g) Cr (ng/g) Cu (ng/g) Mg (lg/g) Mn (ng/g) Pb (ng/g)
Qingdao H. trimaculatus Lips gill 0.12 ±0.00
a
14.0 ±4.71
a
1.39 ±0.50
a
0.83 ±0.40
a
2.67 ±0.15
a
7.23 ±1.74
ab
1.85 ±0.57
a
66.4 ±5.67
a
11.5 ±8.88
a
Visceral mass 0.43 ±0.00
c
23.1 ±0.57
bc
3.95 ±0.04
b
4.93 ±0.17
c
18.6 ±0.90
b
17.0 ±0.14
b
2.00 ±0.01
a
88.8 ±2.83
a
33.6 ±1.24
b
Endoskeleton 0.11 ±0.02
a
24.9 ±1.79
c
14.6 ±1.39
c
2.04 ±0.09
b
5.96 ±0.98
a
41.4 ±9.50
c
1.19 ±0.25
a
82.0 ±13.3
a
20.5 ±0.82
a
Exoskeleton 0.12 ±0.01
a
16.2 ±3.93
ab
3.17 ±0.75
b
1.03 ±0.06
a
6.18 ±2.84
a
5.41 ±1.39
a
1.43 ±0.41
a
38.1 ±2.69
a
15.6 ±5.00
a
Skin 0.19 ±0.04
b
16.7 ±0.67
ab
1.31 ±0.25
a
1.10 ±0.31
a
3.23 ±0.57
a
7.02 ±2.52
ab
1.46 ±0.13
a
59.9 ±3.25
a
17.4 ±0.23
a
Zhoushan H. trimaculatus Brain 0.07 ±0.01
a
14.5 ±3.12
ab
2.82 ±0.88
a
1.61 ±0.95
ab
5.15 ±2.63
a
4.59 ±0.55
a
3.21 ±0.12
c
48.1 ±9.10
a
16.2 ±2.15
a
Lips gill 0.24 ±0.03
b
25.4 ±2.44
bc
2.06 ±0.84
a
1.96 ±0.81
b
17.5 ±6.92
ab
10.6 ±2.78
b
2.98 ±0.66
bc
119.6 ±22.8
b
23.0 ±3.46
a
Visceral mass 0.05 ±0.02
a
5.99 ±0.08
a
2.00 ±0.50
a
0.61 ±0.24
a
24.5 ±4.72
b
6.10 ±1.19
a
2.25 ±0.09
ab
18.0 ±7.57
a
23.2 ±10.4
a
Muscle 0.08 ±0.02
a
31.6 ±10.4
c
1.34 ±0.45
a
1.43 ±0.66
ab
49.3 ±18.6
c
4.55 ±0.76
a
1.40 ±0.40
a
48.7 ±17.8
a
18.6 ±3.35
a
Xiamen H. trimaculatus Lips gill 0.16 ±0.13
cd
16.8 ±2.19
b
1.46 ±0.38
a
1.64 ±0.38
b
2.79 ±0.90
a
5.86 ±0.65
a
1.23 ±0.26
a
57.7 ±17.2
a
14.0 ±5.26
ab
Visceral mass 0.22 ±0.14
d
37.5 ±0.14
c
4.52 ±0.14
b
2.41 ±0.13
c
46.3 ±1.36
d
12.1 ±0.07
c
1.08 ±0.26
a
65.4 ±2.28
ab
19.3 ±0.24
b
Endoskeleton 0.08 ±0.01
a
13.3 ±0.00
ab
3.33 ±1.50
b
0.82 ±0.07
a
14.1 ±8.59
b
6.31 ±0.69
a
2.39 ±0.42
b
55.1 ±7.37
a
13.5 ±1.29
ab
Exoskeleton 0.14 ±0.01
bcd
33.9 ±0.73
c
1.31 ±0.02
a
1.12 ±0.34
a
11.6 ±0.72
b
10.3 ±2.08b
c
2.68 ±0.32
b
67.5 ±8.00
ab
126.6 ±6.73
c
Skin 0.13 ±0.01
abc
12.8 ±1.46
ab
1.54 ±0.60
a
0.86 ±0.09
a
12.3 ±2.08
b
8.21 ±0.62
ab
0.77 ±0.08
a
91.1 ±13.9
b
8.80 ±0.78
a
Muscle 0.09 ±0.01
ab
12.2 ±2.63
a
0.60 ±0.10
a
0.69 ±0.07
a
26.3 ±1.51
c
6.50 ±0.46
a
1.25 ±0.12
a
77.0 ±4.51
ab
7.44 ±0.90
a
H. histrix Brain 0.21 ±0.02
c
19.0 ±1.21
a
3.01 ±0.12
c
2.89 ±0.50
c
17.6 ±0.29
ab
7.48 ±0.19
abc
3.87 ±0.34
c
103.3 ±5.68
c
18.6 ±0.27
abc
Lips gill 0.06 ±0.02
a
14.4 ±5.72
a
2.78 ±1.49
bc
0.61 ±0.08
a
25.5 ±1.23
b
4.40 ±1.76
a
1.09 ±0.02
a
33.6 ±8.49
a
15.0 ±0.61
ab
Visceral mass 0.14 ±0.01
b
17.2 ±3.19
a
1.80 ±1.09
abc
1.16 ±0.39
ab
13.6 ±2.36
ab
8.09 ±1.92
bcd
0.81 ±0.09
a
55.1 ±0.26
ab
24.2 ±3.83
c
Endoskeleton 0.11 ±0.03
b
17.3 ±4.92
a
1.30 ±0.14
ab
1.35 ±0.57
ab
18.7 ±7.33
ab
7.89 ±1.48
bcd
1.02 ±0.01
a
70.8 ±6.53
b
14.7 ±3.31
ab
Exoskeleton 0.14 ±0.02
b
16.9 ±3.45
a
1.99 ±0.49
abc
2.09 ±0.70
bc
7.21 ±2.66
a
9.42 ±1.84
cd
1.82 ±0.55
b
70.1 ±15.0
b
20.5 ±3.15
bc
Skin 0.14 ±0.03
b
19.9 ±9.65
a
1.03 ±0.09
a
1.17 ±0.19
ab
23.1 ±1.20
b
5.48 ±0.63
ab
1.29 ±0.26
ab
50.6 ±12.9
ab
12.1 ±2.81
a
Muscle 0.11 ±0.01
b
11.4 ±3.48
a
2.21 ±0.88
abc
0.79 ±0.04
a
20.8 ±4.83
ab
11.0 ±1.20
d
0.77 ±0.03
a
52.5 ±7.78
ab
12.9 ±4.81
a
Shanwei H. kuda Visceral mass 0.12 ±0.05
a
13.3 ±2.49
a
1.00 ±0.06
a
1.26 ±0.01
ab
29.5 ±2.83
d
10.7 ±1.46
b
3.02 ±0.01
b
38.9 ±1.72
a
21.6 ±10.5
b
Endoskeleton 0.14 ±0.27
ab
53.5 ±10.2
c
2.25 ±0.29
c
2.48 ±1.15
b
4.74 ±1.20
a
7.23 ±2.41
a
3.91 ±0.31
c
68.3 ±17.5
c
23.4 ±2.02
b
Exoskeleton 0.19 ±43.4
b
24.1 ±3.01
b
0.95 ±0.01
a
1.29 ±0.51
ab
14.0 ±3.02
b
4.11 ±1.05
a
1.89 ±0.19
a
44.1 ±1.55
ab
14.3 ±5.74
ab
Skin 0.15 ±0.01
a
16.9 ±1.41
ab
1.77 ±0.30
bc
1.06 ±0.31
a
21.3 ±1.28
c
27.5 ±0.80
c
2.78 ±0.21
b
40.7 ±8.82
a
10.7 ±3.15
a
Muscle 0.09 ±0.02
a
12.3 ±2.87
a
1.26 ±0.41
ab
1.32 ±0.25
ab
5.10 ±0.70
a
4.21 ±0.89
a
1.39 ±0.29
a
62.9 ±1.39
bc
24.8 ±3.16
b
Zhanjiang H. trimaculatus Lips gill 0.31 ±0.04
b
29.8 ±1.47
b
1.91 ±0.11
a
2.55 ±0.45
d
13.0 ±0.46
b
10.5 ±0.95
c
3.16 ±0.35
c
178.5 ±9.45
c
20.1 ±0.67
bc
Visceral mass 0.13 ±0.03
a
8.87 ±0.72
a
2.04 ±0.22
a
0.99 ±0.12
a
4.30 ±0.65
a
6.08 ±0.97
a
1.63 ±0.13
ab
48.6 ±1.23
a
12.0 ±0.58
a
Endoskeleton 0.14 ±0.05
a
20.4 ±1.56
ab
3.52 ±0.77
b
1.81 ±0.22
c
7.34 ±2.64
ab
9.13 ±1.43
bc
1.41 ±0.12
ab
180.6 ±11.5
c
23.9 ±3.95
c
Exoskeleton 0.12 ±0.01
a
16.5 ±1.16
ab
5.97 ±0.55
c
1.53 ±0.16
bc
10.4 ±3.91
b
9.12 ±1.13
bc
1.08 ±0.01
a
40.9 ±3.58
a
36.1 ±1.23
e
Skin 0.10 ±0.02
a
24.3 ±2.79
ab
2.33 ±0.49
a
1.15 ±0.27
ab
7.60 ±4.22
ab
7.88 ±1.66
ab
2.00 ±0.70
b
58.7 ±23.8
a
15.7 ±3.82
ab
Muscle 0.29 ±0.03
b
16.9 ±0.70
ab
7.71 ±0.35
d
3.22 ±0.41
e
13.2 ±0.74
b
20.6 ±0.96
d
1.08 ±0.26
a
104.5 ±14.3
b
30.3 ±0.46
d
H. kelloggi Brain 0.12 ±0.04
ab
15.7 ±0.36
b
10.1 ±0.17
b
1.29 ±0.09
a
8.58 ±0.24
a
6.43 ±1.21
a
0.96 ±0.32
a
86.4 ±22.2
a
12.8 ±1.66
ab
Lips gill 0.12 ±0.01
ab
17.1 ±4.78
b
1.45 ±0.74
a
1.40 ±0.54
a
16.6 ±0.69
ab
6.99 ±1.51
a
1.19 ±0.10
ab
57.7 ±3.26
a
13.1 ±3.10
ab
Visceral mass 0.08 ±0.01
a
7.22 ±0.15
a
3.24 ±0.12
a
1.04 ±0.02
a
4.72 ±0.23
a
0.93 ±0.05
a
60.9 ±4.12
a
11.8 ±1.23
a
Endoskeleton 0.26 ±0.06
c
21.8 ±3.24
bc
5.08 ±1.38
a
3.41 ±0.74
b
12.9 ±2.29
a
14.2 ±1.16
b
1.22 ±0.09
ab
112.5 ±5.79
ab
35.8 ±6.81
d
Exoskeleton 0.19 ±0.03
bc
16.7 ±3.41
b
1.71 ±0.45
a
1.46 ±0.50
a
6.46 ±1.86
a
6.97 ±1.84
a
1.31 ±0.07
ab
125.4 ±20.9
ab
20.7 ±8.77
abc
Skin 0.36 ±0.08
d
41.9 ±6.87
d
3.02 ±0.15
a
2.84 ±0.91
b
7.10 ±1.50
a
18.9 ±5.11
c
1.98 ±1.47
b
261.4 ±3.56
b
25.7 ±6.42
bcd
Bull Environ Contam Toxicol
123

liver for accumulating pollutants from their environment
(Galindo et al. 1986), and the specific metabolism process
and the enzyme-catalyzed reaction involved Cd, Cu, Mn,
and Zn take place at liver in fish (Jaffar and Pervais Shahid
1989). These results were similar to the reports for tilapia,
which had high metal concentrations in muscle because
these fish mainly feed on demersal foods and sediments
(Zhou and Wong 2000; Nakayama et al. 2010). So far, very
few studies have concerned the relationship between the
prey type and bioaccumulation of metals for seahorses in
the wild.
Acknowledgments This study was funded by the Outstanding
Youth Foundation in Guangdong Province (S2013050014802), the
National Science Fund for Excellent Young Scholars (41322038), the
National Natural Science Foundation of China (41176146,
41306148), and the Special Fund for Agro-scientific Research in the
Public Interest (201403008).
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Table 2 continued
Locations Species Tissues Metal concentrations
Al (lg/g) Ba (ng/g) Cd (ng/g) Ce (ng/g) Cr (ng/g) Cu (ng/g) Mg (lg/g) Mn (ng/g) Pb (ng/g)
Muscle 0.23 ±0.01
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0.82 ±0.07
a
37.7 ±8.64
a
10.1 ±2.99
a
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ab
12.2 ±7.68
a
1.18 ±0.11
ab
1.24 ±0.96
a
16.9 ±2.13
b
13.9 ±6.19
b
1.18 ±0.09
ab
48.4 ±29.7
ab
15.1 ±1.27
ab
Exoskeleton 0.13 ±0.03
a
27.9 ±3.85
a
2.81 ±1.37
ab
0.99 ±0.18
a
8.70 ±4.62
a
11.9 ±6.59
ab
2.36 ±0.15
b
62.8 ±11.8
abc
26.1 ±4.23
b
Skin 0.27 ±0.04
c
19.6 ±7.10
a
1.08 ±0.34
ab
2.18 ±0.61
a
9.25 ±0.98
a
7.88 ±3.04
ab
1.70 ±0.49
ab
57.9 ±14.0
abc
22.0 ±6.18a
b
Muscle 0.15 ±0.02
ab
15.3 ±0.70
a
3.44 ±1.91
b
1.39 ±0.27
a
14.0 ±4.31
ab
7.90 ±2.33
ab
1.55 ±0.33
ab
92.8 ±29.6
c
21.2 ±0.34
ab
Data are mean ±SD (n =9). For each metal, different letters indicate significant differences among different tissues (p\0.05)
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