Methylmercury in fish from the South China Sea: Geographical distribution and biomagnification

Marine Pollution Bulletin 77 (2013) 437–444

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Methylmercury in fish from the South China Sea: Geographical distribution and biomagnification Aijia Zhu a,b,c, Wei Zhang a, Zhanzhou Xu c, Liangmin Huang a, Wen-Xiong Wang d,⇑ a

Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China University of Chinese Academy of Sciences, Beijing 100049, China c South China Sea Environmental Monitoring Center, State Oceanic Administration, Guangzhou 510300, China d Division of Life Science, The Hong Kong University of Science and Technology (HKUST), Clear Water Bay, Kowloon, Hong Kong b

a r t i c l e

i n f o

Keywords: Methylmercury Bioaccumulation Biomagnification Marine fish South China Sea

a b s t r a c t We conducted a large-scale investigation of methylmercury (MeHg) in a total of 628 marine wild fish covering 46 different species collected from the South China Sea between 2008 and 2009. Biological and ecological characteristics such as size (length and wet weight), feeding habit, habitat, and stable isotope (d15N) were examined to explain MeHg bioaccumulation in marine fish and their geographical distribution. MeHg levels in the muscle tissues of the 628 individuals ranged from 0.010 to 1.811 lg/ g dry wt. Log10 MeHg concentration was significantly related to their length and wet weight. Feeding habit and habitat were the primary factors influencing MeHg bioaccumulation. Demersal fish were more likely to be contaminated with MeHg than the epipelagic and mesopelagic varieties. Linear relationships were obtained between Log10 (MeHg) and d15N only for one location, indicating that biomagnification was site-specific. Results from this study suggest that dietary preference and trophic structure were the main factors affecting MeHg bioaccumulation in marine fish from the South China Sea. Ó 2013 Elsevier Ltd. All rights reserved.

Mercury (Hg) is recognized as an important pollutant since it can cycle globally and poses risks to humans and ecosystems. Emission inventories have indicated that Asian Hg sources account for more than 50% of the global anthropogenic total Hg (THg) (Jaffe et al., 2005; Zhang and Wong, 2007). Because of the rapid economic growth, Hg emissions in China grew quickly at a rate of 5.1% during the period of 1995–2005 (Streets et al., 2009), and the country is now responsible for 25% of worldwide Hg emission. The major sources of Hg in the environment in China are Hg production, coal combustion, and industrial sources (Tang et al., 2007). A critical aspect of Hg cycling is its bioaccumulation and methylation (Amlund et al., 2007; Munthe et al., 2007). Once it enters aquatic ecosystems, a portion of the Hg can be methylated by bacteria (Swain et al., 2007). Methylmercury (MeHg) is considered as a neurotoxin, and its developmental neurotoxicity to the fetus constitutes the current basis for risk assessments and public health policies as indicated by the Madison Declaration on Mercury Pollution (Hurley et al., 2007). Humans and wildlife are most commonly exposed to MeHg through the consumption of fish from marine and freshwater sources (Swain et al., 2007; Zhang and Wong, 2007). Unlike the concentrations of most other trace metals, the concentrations of Hg, especially MeHg, increase along the marine food ⇑ Corresponding author. Tel.: +852 23587346; fax: +852 23581559. E-mail address: [email protected] (W.-X. Wang). 0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2013.09.009

chain through biomagnification. Consequently, d15N has been used to estimate the biomagnification of Hg in marine and aquatic food webs in the last decade (Mackintosh et al., 2004). Bioaccumulation and biomagnification of THg and MeHg concentrations in fish are generally influenced by fish size (Mason et al., 2006; Kehrig et al., 2008), trophic position (as indicated by d15N) (Amlund et al., 2007; Mergler et al., 2007; Sharma et al., 2008), and life history (Swanson et al., 2011). Furthermore, Hg levels in fish also vary by geographic area (Kamman et al., 2005; Al-Reasi et al., 2007; Kinghorn et al., 2007). For these reasons the concentration and behaviour of Hg in aquatic systems have been of great interest and importance. Compared to the situation for many freshwater fishes and ecosystems, there are relatively fewer monitoring data for Hg in marine fishes (Anonymous, 2007). Valid data on the MeHg concentration in fish of different species and information on the sources of MeHg to estuaries, coastal zones, and particularly the oceans are still limited, especially on a local level (Burger and Gochfeld, 2006; Munthe et al., 2007). In China, few studies have focused on MeHg bioaccumulation in fish, especially marine fish from tropical areas such as the South China Sea (Zhang and Wong, 2007). Marine fish consumption is currently a major route for human exposure to Hg in Chinese coastal cities (Liu et al., 2008), but few people are aware of it. The objective of this study was to quantify MeHg in different marine wild fish species from different regions around the South

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China Sea, and to determine the influence of biological and ecological factors (e.g. length, wet weight, feeding habit, habitat, and regional distribution) on the bioaccumulation of Hg in the muscle tissues of marine wild fish. Given the human and environmental health concerns of MeHg, it is critical to understand the spatial distribution of its production and fate in marine ecosystems. Data on Hg concentration in marine fish are necessary for estimating the national exposure, evaluating the potential risks of fish consumption, and issuing consumers advice. Between October 2008 and June 2009, a total of 628 fish samples belonging to 46 species (mostly common edible fish) were collected from the South China Sea (Fig. 1). Samples from the Pearl River Estuary were captured with trawls while samples from the coral reef waters of Xisha Islands and Nansha Islands were caught with rod and line. Samples from other coastal areas, including Shantou, Beihai and Sanya coastal waters, were purchased from local fishermen as soon as the fish were caught. All samples were transported frozen or ice-cold to the laboratory where they were kept at 20 °C until further treatment. In the laboratory, we determined the fish length and body weight, and then the skinless white dorsal muscle tissues were removed with clean scalpels and weighed (wet weight). Following weighing, muscle tissues stored in sealed plastic bags were freeze-dried. The dry weight of each muscle tissue was determined in order to calculate the wet/dry weight (W/D) ratio of each sample. Then they were homogenized and kept dry until analysis.

MeHg in fish was extracted by digesting approximately 20 mg of dry tissues with 25% KOH in methanol at 85 °C for 4 h. The extracted fish tissues were buffered with sodium acetate at pH 4.9, and ethylated by sodium tetraethylborate in a 40 mL Teflon line borate glass bottle. The quantification of MeHg was carried out by the automated methylmercury analytical system (MERX, Brooks Rand). The quality of MeHg determination was ensured by conducting replicate assays for 20% of the samples (SD < 10%) and analysis of the standard reference material NIST SRM 1566b, oyster tissue (13.2 ± 0.7 ng/g) and IAEA 142 (No. 55) muscle tissue (47 ng/ g), with recovery rates of 90–98%. MeHg concentrations were expressed on a dry-weight basis and appropriately converted using the wet weight/dry weight ratio when comparing with other data reported on a wet-weight basis. The 15N/14N of a powdered sample was analyzed using an elemental analyzer coupled to a Delta XL Plus mass spectrometer (Finnigan). Samples were added into tin capsules and combusted in a flow of helium to reduce all forms of nitrogen to pure N2. The pure gas was then separated on a gas chromatographic column before being injected into the mass spectrometer. Isotopic ratio was reported in part per thousand (‰) relative to the standard (atmospheric nitrogen) and was defined in delta notation as:

d15 N ¼ ðRsample =Rstandard  1Þ  103 where R = 15N/14N. Most biota was spheric dinitrogen.

Fig. 1. Locations of sampling sites in the coastal coral reef waters of the South China Sea.

15

N-enriched versus atmo-

A. Zhu et al. / Marine Pollution Bulletin 77 (2013) 437–444

Trophic level and trophic magnification factor (TMF) were estimated from d15N ratio using the following equations (Coelho et al., 2013):

TL ¼ ½ðd15 Nspecies  d15 Nbase Þ=Dd15 N þ TLbase TMF ¼ 10b where TL is the trophic level, d15Nspecies is the d15N signature of the fish species in question, d15Nbase is the d15N signature of a representative baseline and TLbase is the trophic level of that baseline. Dd15N assumes a trophic fractionation of 3.4‰ per trophic level (Post, 2002). Because there was no data on the primary producers in this study, the herbivorous species Siganus canaliculatus with TL = 2 was used as the baseline to calculate the trophic levels of other species. For TMF estimation, b is the slope of linear regression between logtransformed MeHg concentration and d15N. Individual age was estimated for some species using growth parameters or average sizes of each age class available from the literatures (Chen and Qiu, 2003; Qiu et al., 2008; Lu and Chen, 2008; Chien, 2009; Liu et al., 2010). Statistical analysis was performed using SPSS 16.0 for Windows (SPSS Inc., USA). Pearson correlation was used to determine the relationship between MeHg concentration in fish muscle and biological parameters (length and wet weight). Significance was accepted when p < 0.05. Analysis of variance (ANOVA), t-test and Duncan’s significant difference test were conducted in order to analyze the differences in MeHg across species and locations. A linear regression model was used to test the relationship between fish muscle MeHg and biological parameters or d15N. The data were log-transformed. Detailed results on inter-specific differences are presented in Table 1. Means of MeHg concentrations in marine fish muscles ranged from 0.010 lg/g dry wt (Exocoetus sp.) to 1.811 lg/g dry wt (Sargocentron caudimaculatum). Several specific trends were observed. In Shantou, the MeHg concentrations in Johnius belangerii (0–3 year old), Nemipterus virgatus (1–2 year old), Trichiurus sp., Trypauchen vagina (mainly 0–2 year old) were significantly higher than those in other fish species (mainly 0–3 year old). In the Pearl River Estuary, there was no significant difference in MeHg concentrations among different fish species. In Beihai, Evynnis cardinalis (mainly 0–1 year old) had significantly higher MeHg levels than the other fish species, but the other fish species were not significantly different. In Sanya, the highest MeHg levels were found in S. caudimaculatum, followed by J. belangerii (mainly 2–3 year old) and Terapon theraps (2–3 year old), which may have been due to their relatively old ages (Table 2) since MeHg may increase with age (Coelho et al., 2013). S. caudimaculatum had the highest individual MeHg concentration, with 1.811 lg/g dry wt of MeHg found in one sample. There was no significant difference among the other fish species found in the region. The mean MeHg concentrations in all species were below the recommended level of 0.30 lg/g wet wt in fish tissue based on the consumption rate of the US population (US Environmental Protection Agency, 2001), except those in two individuals of J. belangerii and four individuals of S. caudimaculatum from the Sanya coastal area. In the present study, the length and wet weight of the marine wild fish species varied from 4.9 to 37.5 cm and 1.8 to 711.2 g, respectively. Linear regressions between MeHg concentration in marine fish muscles and individual length or wet weight were established for each species from different sites. Significant relationships (p < 0.05) were observed between MeHg concentration and length of 13 marine fish species from Shantou, Pearl River Estuary, Beihai and Sanya (Table 3). Moreover, MeHg in 9 marine fish species from the above 4 sites was significantly related to their wet weights (Table 3). However, the relationship between MeHg concentration and length of Sillago sihama from Shantou was

439

negative. No trend was observed in other species in this study, probably due to the small size range sampled in the same species of fish. The positive relationship between the MeHg concentration and fish size (length and wet weight) was consistent with numerous previous studies (Sonesten, 2003; Trudel and Rasmussen, 2006; Storelli et al., 2007; Staudinger, 2011). Storelli et al. (2002), for example, reported that size and Hg levels were highly correlated for swordfish (Xiphias gladius) and bluefin tuna (Thunnus thynnus) from the Mediterranean Sea. Walters et al. (2010) suggested that body size and trophic guild were the best predictors of Hg concentrations, which were the highest in large-bodied apex predators. At least two compatible mechanisms have been hypothesized to be responsible for this pattern. First, the slow rate of elimination of MeHg by fish relative to its rapid uptake leads to an increase in the MeHg concentration in fish muscle tissue with size (length and weight) even if dietary concentrations of Hg remain constant (Wiener et al., 2003). Second, fish undergo ontogenetic diet shifts to prey occupying higher trophic positions as they grow, thereby exposing themselves to higher concentrations of MeHg (Stafford et al., 2004; Davis et al., 2008). Recently, Dang and Wang (2012) investigated the biokinetic factors leading to the body size dependence of Hg concentration in the juvenile blackhead seabream Acanthopagrus schlegeli. They quantified the key size-dependent biokinetic parameters for MeHg, including the dissolved uptake rate constant, assimilation efficiency and the elimination rate constant. Among the examined kinetic parameters, growth rate and Hg elimination differences collectively explained most of the sizedependence of Hg concentration. Specifically, the slower growth and elimination of Hg in larger fish may account for the increasing concentrations of Hg in the fish. Trudel and Rasmussen (1997) also reported that the Hg elimination rate was negatively related to size. In addition to body size, MeHg concentration variances might also be related to feeding habit and habitat. In our study, the different marine fish species mainly fed on plankton (phytoplankton and zooplankton), crustaceans, shrimp, small fish, and benthic invertebrates (polychaete). Higher MeHg concentrations (>0.2 lg/g) were observed for species exclusively feeding on diets of small fish, shrimp, crustaceans and benthic invertebrates. These species were E. cardinalis (0–1 year old), J. belangerii (mainly 0–3 year old), N. virgatus (0–2 year old), Polydactylus sextarius, S. caudimaculatum, and T. theraps (2–3 year old) collected from Shantou, Beihai and Sanya. Their MeHg concentrations (0.211–1.179 lg/g) were significantly higher than those of the planktivorous and herbivorous species (0–3 year old, 0.015–0.154 lg/g, t-test, p < 0.0001) from Shantou, Pearl River Estuary, Beihai and Sanya (Tables 1 and 2). In natural environment, fish are primarily exposed via the trophic route, which is strongly dependent on the diet of the species. Interspecies differences in diet likely account for the observed patterns of Hg bioaccumulation (Bank et al., 2007; Piraino and Taylor, 2009). Hammerschmidt and Fitzgerald (2006) also reported that the fish concentration of MeHg depends largely on the selection of prey items, and ontogenetic shifts in feeding habit can also influence MeHg concentration. The habitats of marine fish could also be responsible for the variability in MeHg concentration in the fish muscles analyzed. In the present study, the marine fish were coastal, epipelagic and mesopelagic, demersal, and reef species. The MeHg concentrations (0.015–0.045 lg/g) in epipelagic, mesopelagic and rock fish species such as Clupanodon thrissa (3 year old), Decapterus maruadsi (0–1 year old), Hyporhamphus dussumieri, and S. canaliculatus were lower than the MeHg concentrations (0.022–0.280 lg/g) in demersal fishes (0–3 year old) from Shantou. Similar results were also found for Pearl River Estuary and Beihai. The situation in Sanya was somewhat different, and high MeHg concentration was found in the rock species S. caudimaculatum. When this species was

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Table 1 MeHg concentrations (dry-weight basis), d15N values, trophic level, feeding types and habitat depths in marine wild fish species collected from different locations of the South China Sea. Data are mean ± SD. Different alphabets indicate significant differences among fish species in the same location (p < 0.05). Location

Species

Feeding type

Depth

Shantou

Clupanodon thrissa

Plankton

Epipelagic and mesopelagic, 0–60 m Epipelagic and mesopelagic, 0– 100 m Demersal, 20–240 m

Decapterus maruadsi Dipturus kwangtungensis Hyporhamphus dussumieri Johnius belangerii Nemipterus virgatus Paraplagusia japonica Pardachirus pavoninus Pleuronichthys cornutus Scorpaena neglecta Siganus canaliculatus Sillago sihama Thamnaconus hypargyreus Trichiurus sp. Trypauchen vagina Iniistius verrens Pearl River Estuary

Zooplankton Carnivorous (crustaceans, benthic worms) Carnivorous (benthic crustaceans, fish) Benthic invertebrates

Demersal, 220 m Demersal, 20–65 m

7

12.8 ± 0.4

Weight (g)

MeHg (lg/ g dry wt)

d15N (‰)

Trophic levela

41.5 ± 5.9

0.024 ± 0.007a

11.86

2.2

a

11.89

2.2

6

16.1 ± 0.6

75.6 ± 5.9

0.045 ± 0.012

7

14.4 ± 0.6

117.1 ± 10.7

0.124 ± 0.019a

11.75

2.2

a

12.70

2.5

b

14.38

3.0

5

17.6 ± 1.0

47.1 ± 7.5

0.015 ± 0.006

50

12.6 ± 2.5

45.7 ± 22.2

0.224 ± 0.144

6

17.6 ± 0.6

113.6 ± 14.1

0.274 ± 0.168b

13.18

2.6

10

13.2 ± 1.1

23.7 ± 5.4

0.072 ± 0.028a

11.31

2.1

a

11.73

2.2

Demersal, coral reef, 2–40 m Demersal, 100–120 m

10

9.5 ± 0.4

20.8 ± 2.8

0.106 ± 0.038

3

14.4 ± 0.5

88.2 ± 1.8

0.037 ± 0.010a

11.58

2.1

Carnivorous (crustaceans, small fish) Herbivorous (benthic plants)

Rock, demersal, 100– 150 m Rock, coral reef, 1– 50 m Demersal, 0–60 m

8

11.2 ± 0.5

42.0 ± 3.5

0.022 ± 0.010a

12.52

2.4

0.032 ± 0.011

a

11.10

2.0

a

13.89

2.8

Carnivorous (polychaete worms, shrimps) Carnivorous (benthic organisms) Crustaceans, cephalopod, fish Carnivorous (benthic invertebrates) carnivorous (crustaceans) Carnivorous (shrimp, small fish)

Lateolabrax japonicus Mugil cephalus

Carnivorous

Taenioides anguillaris Trypauchen vagina

Epipelagic and mesopelagic, 1–30 m Demersal, 1–40 m

Length (cm)

Carnivorous (benthic crustaceans) Carnivorous (benthic organisms)

Acentrogobius chlorostigmatoides Acentrogobius sp. Coilia mystus Konosirus punctatus

Odontamblyopus lacepedii Onigocia macrolepis Sardinella albella Siganus canaliculatus Sillago sihama

Beihai

Zooplankton

n

Small invertebrates Plankton

omnivorous (zooplankton, benthic organisms, detritus) Carnivorous (crustaceans, small fish) Carnivorous (small fish, invertebrates) Plankton Herbivorous (benthic plants) Carnivorous (polychaete worms, shrimps)

Demersal, 50–100 m Mesopelagic, demersal Demersal demersal, 5–20 m

18

14.1 ± 0.8

62.0 ± 11.2

11

10.6 ± 0.3

13.3 ± 1.8

0.062 ± 0.026

8

13.6 ± 0.3

52.0 ± 5.0

0.073 ± 0.018a

10.92

1.9

28

15.1 ± 1.1

50.5 ± 12.2

0.280 ± 0.096b

15.08

3.2

b

13.22

2.6

12

13.6 ± 2.2

14.7 ± 8.4

0.184 ± 0.132

0.055 ± 0.017a

11.11

2.0

0.089 ± 0.040cd

14.96

2.4

0.136 ± 0.052e 0.064 ± 0.028abcd 0.045 ± 0.010ab

13.96 15.92 15.32

2.1 2.7 2.5

7

11.4 ± 0.3

32.3 ± 2.2

Demersal

33

7.2 ± 1.2

7.5 ± 3.7

Demersal Pelagics, 0–20 m Epipelagic and mesopelagic, 10– 50 m demersal, 5–30 m

11 14 12

6.7 ± 0.7 11.0 ± 1.3 10.1 ± 0.7

5.1 ± 1.9 5.7 ± 2.0 18.6 ± 3.8

4

7.7 ± 0.4

8.4 ± 1.4

0.042 ± 0.011a

19.60

3.8

Demersal, 0–120 m

12

12.4 ± 2.6

26.5 ± 16.6

0.104 ± 0.042de

Benthopelagic

23

14.8 ± 2.5

9.5 ± 3.8

Demersal, 5–100 m

3

10.8 ± 1.0

9.2 ± 4.4

Pelagic, 0–50 m Rock, coral reef, 1– 50 m Demersal, 0–60 m

13 10

9.7 ± 0.5 11.2 ± 0.7

15.4 ± 2.6 28.7 ± 3.6

14

9.5 ± 1.0

9.4 ± 3.1

11.87

1.5

0.085 ± 0.048

bcd

12.20

1.6

0.037 ± 0.016

a

15.86

2.7

0.143 ± 0.041e 0.038 ± 0.008a

12.86 13.61

1.8 2.0

0.054 ± 0.019abc

3.5

16.00

2.7

Demersal

5

17.3 ± 4.6

18.1 ± 15.5

Carnivorous (benthic invertebrates)

Demersal

4

10.0 ± 0.3

5.8 ± 0.6

0.045 ± 0.008ab

17.45

3.1

Branchiostegus argentatus Decapterus maruadsi

Carnivorous (small fish, benthic organisms) Zooplankton

Demersal, 51–65 m

25

15.6 ± 2.3

74.6 ± 35.4

0.125 ± 0.047cd

13.62

–

cd

11.65

–

Evynnis cardinalis

Carnivorous (fish, shrimp, mollusk) Zooplankton Carnivorous (crustaceans, small fish) Crustaceans, cephalopod, fish

Exocoetus volitans Nemipterus virgatus Trichiurus sp. Sphyraena pinguis Siganus canaliculatus

Carnivorous (small fish) Herbivorous (benthic plants)

0.104 ± 0.032

18.70

de

Epipelagic and mesopelagic, 0– 100 m demersal, 5–100 m

14

14.6 ± 1.0

39.0 ± 10.0

0.127 ± 0.035

14

11.8 ± 2.0

53.9 ± 5.7

0.278 ± 0.105f

13.21

–

Pelagics, 0–20 m Demersal, 40–220 m

17 19

20.0 ± 0.8 10.6 ± 1.4

126.4 ± 14.2 31.7 ± 12.1

0.105 ± 0.034bcd 0.148 ± 0.070de

10.49 14.37

– –

Mesopelagic, demersal, 0–200 m Pelagic, 3–6 m Rock, coral reef, 1– 50 m

26

22.3 ± 6.9

227.5 ± 161.5

0.188 ± 0.061cd

12.57

–

8 6

22.0 ± 1.8 14.1 ± 0.8

101.2 ± 23.9 54.9 ± 10.6

0.179 ± 0.033e 0.062 ± 0.025ab

14.85 14.27

– –

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A. Zhu et al. / Marine Pollution Bulletin 77 (2013) 437–444 Carnivorous (small fish, crustaceans) Carnivorous (small fish, crustaceans)

Demersal, 30–60 m

12

12.5 ± 0.8

76.5 ± 13.4

0.036 ± 0.010a

14.56

–

Rock, coastal waters, 5–10 meres

14

13.8 ± 0.5

52.6 ± 5.5

0.081 ± 0.013bc

14.60

–

Ariomma indicum Branchiostegus auratus Decapterus maruadsi

Carnivorous (invertebrates) Carnivorous (small fish, shrimp)

Demersal, 20–300 m Demersal, 50–200 m

6 6

11.6 ± 0.3 14.3 ± 1.1

48.6 ± 3.4 52.0 ± 9.8

0.057 ± 0.007ab 0.151 ± 0.020abc

12.03 11.99

2.1 2.1

Zooplankton

4

16.3 ± 0.5

74.8 ± 14.3

0.154 ± 0.047abc

12.78

2.3

Evynnis cardinalis

Carnivorous (fish, shrimp, mollusk) Carnivorous (crustaceans, benthic worms) Plankton

Epipelagic and mesopelagic, 0– 100 m Demersal, 5–100 m

10

11.4 ± 0.7

59.1 ± 8.7

0.269 ± 0.089c

13.53

2.5

Demersal, 1–40 m

9

15.7 ± 0.7

81.2 ± 10.6

0.903 ± 0.322e

Psenopsis anomala Trachurus japonicus Sanya

Johnius belangerii Konosirus punctatus Mene maculata Nemipterus virgatus Polydactylus sextarius Sargocentron caudimaculatum Siganus canaliculatus Terapon theraps Xisha Islands

Amblyglyphidodon curacao Apogonichthys sp. Caesio caerulaurea Chaetodon rafflesii Gnathodentex aureolineatus Zanclus cornutus

Nansha Islands

Gnathodentex aureolineatus Cephalopholis spiloparaea Parapercis pacifica Exocoetus sp.

Carnivorous (zooplankton, benthic invertebrates) Carnivorous (benthos crustaceans, fish) Carnivorous (shrimps, fishes, benthic organisms) Carnivorous (benthic shrimp, crustaceans) Herbivorous (benthic plants) carnivorous (small fish, invertebrates)

Pelagic, 10–50 m

Rock, coral reef, 2– 40 m Rock, coral reef, 1– 50 m Demersal, 1–30 m

2.2

11.94

2.0

10

12.9 ± 0.6

55.6 ± 6.9

0.092 ± 0.015

9

13.7 ± 0.5

74.8 ± 8.2

0.082 ± 0.032abc

10.57

1.6

8

10.4 ± 1.5

30.8 ± 14.3

0.180 ± 0.059abc

Rock, coastal waters, 20–95 m Demersal, 220 m Demersal, 19–73 m

12.52

abc

12

12.8 ± 1.1

46.6 ± 12.9

0.211 ± 0.120

11.88

2.0

bc

14.40

2.8

f

13.10

2.4

9

16.3 ± 2.2

187.3 ± 37.9

1.179 ± 0.438

14

12.5 ± 0.7

37.7 ± 5.1

0.039 ± 0.017a

11.78

2.0

11

12.9 ± 0.9

58.2 ± 13.4

0.554 ± 0.209d

12.82

2.3

Zooplankton, fila

Coral reef, 1–40 m

1

6.9

18.8

0.057

10.38

–

Carnivorous (zooplankton, benthic invertebrates) Zooplankton Carnivorous (sea anemones, polychaetes, coral polyps) Carnivorous (benthic invertebrates) Small encrusting animals

Coral reef, 1–65 m

1

5.4

6.2

0.164

11.80

–

Coral reef, 5–50 m Coral reef, 1–15 m

1 1

13.4 5.2

50.0 6.8

0.034 0.059

8.63 9.90

– –

Coral reef, 3–30 m

1

12.8

59.8

0.084

10.98

–

Carnivorous (benthic invertebrates)

Zooplankton

Coral reef, 1–180 m

1

5.6

7.7

0.041

6.18

–

Coral reef, 3–30 m

1

14.4

73.7

0.495

9.95

–

Coral reef, 30–108 m

1

12.0

29.4

0.249

9.76

–

Benthopelagic, 0–6 m Pelagic, 0–20 m

1 2

13.5 13.2 ± 0.6

41.5 35.5 ± 4.6

9.09 8.15

– –

0.278 0.022 ± 0.017

a Herbivorous species (Siganus canaliculatus) was only collected in Shantou, Pearl River Estuary and Sanya. Thus, trophic level was only estimated for species from the above three locations.

excluded from the analysis, the demersal species from Sanya had statistically higher MeHg concentrations than those in epipelagic, mesopelagic and rock species (p < 0.001). Given that demersal fish live and feed near the bottom of the sea, they may accumulate more Hg through trophic transfer process. Monteiro et al. (1996) reported that fish from greater depths showed heighted levels of Hg, with the mesopelagic species possessing higher Hg concentrations than the epipelagic species. It was difficult to clearly assess the regional differences in MeHg contamination using all fish samples, mainly because the same species could not be collected from all locations. Therefore, we chose 8 species (D. maruadsi, E. cardinalis, J. belangerii, Konosirus punctatus, N. virgatus, S. canaliculatus, S. sihama, and T. vagina), which were collected from more than one location, to analyze the geographical variance among Shantou, Pearl River Estuary, Beihai and Sanya. Through one-way ANOVA analysis, the MeHg concentrations in D. maruadsi (1 year old), J. belangerii (2–3 year old) and K. punctatus (1 year old) from Sanya were significantly higher than those from other locations (p < 0.001), whereas the lowest MeHg concentrations in D. maruadsi (1 year old) and J. belangerii (0–3 year old) were detected from Shantou. Interestingly, we found that the MeHg concentrations in D. maruadsi at the same age class were the highest down south (Sanya) and the lowest up north (Shantou).

Table 2 Age of six species from different locations in the South China Sea. Species

Clupanodon thrissa Coilia mystus Decapterus maruadsi Dipturus kwangtungensis Evynnis cardinalis Johnius belangerii Konosirus punctatus Nemipterus virgatus Sillago sihama Terapon theraps Trypauchen vagina

Location Shantou

Pearl River Estuary

Beihai

Sanya

3 – 1 1–3 – 0–3 – 1–2 1–2 – 0–2c

– 0–1 – – – – – – 0–2 – 0–1

– – 0–1 – 0–1a – – 0–1 – – –

– – 1 – 0–1 2–3b 1 1–2 – 2–3 –

‘‘–’’ No sample. a Except one individual >2 years old. b Except two individuals >4 years old. c Except two individuals >3 years old.

The Pearl River Estuary is considered to be the most eutrophic area in the South China Sea, which, together with the relative small size of K. punctatus (0–1 year old), may explain the significantly lower Hg levels found in that area than those from Sanya (1 year

A. Zhu et al. / Marine Pollution Bulletin 77 (2013) 437–444

old) (p < 0.001). Beihai showed higher MeHg concentrations in D. maruadsi (0–1 year old, with smaller size) than those from Shantou (1 year old), due possibly to the coal combustion and industrial discharge activities in nearby provinces. Beihai is a city in Guangxi Province, which is bordered by Guizhou Province to the north and Yunnan Province to the west. The latter two provinces have been shown to emit large amounts of Hg from coal combustion (Wang et al., 1999). In particular, very high levels of gaseous elemental Hg in the atmosphere and high soil Hg content have been recorded in Guiyang City, the provincial capital city of Guizhou Province (Zhang and Wong, 2007). Thus, the high Hg concentrations in D. maruadsi collected from the Beihai coastal area may be associated with the high Hg emissions from the adjacent inland provinces to some extents. A previous study has shown that Hg concentrations in many food items found in Guizhou Province exceeded the safe consumption limits (Chen et al., 1999). High MeHg level in J. belangerii and K. punctatus from Sanya may be due to the larger size and older age than those from Shantou or Pearl River Estuary. However, it is difficult to explain the higher Hg concentrations in D. maruadsi collected from the Sanya coastal waters than those from Shantou with similar sizes, since information on the environmental characteristics, environmental Hg concentrations and food web in that area is limited. Migration of fish species for feeding and reproduction may affect the MeHg geographical differences. Further studies to identify the source of Hg in the Sanya coastal waters are required. The d15N of fish from different sampling sites ranged from 8.15‰ in Exocoetus sp. (from Nansha Islands) to 19.6‰ in Lateolabrax japonicus (from the Pearl River Estuary) (Table 1), representing an 11‰ variation. Log10 MeHg concentrations showed significantly positive correlations with d15N in Shantou (Fig. 2), indicating an overall biomagnification of MeHg. Surprisingly, Log10 MeHg was significantly and negatively related to d15N in the Pearl River Estuary. No relationship was found between Log10 MeHg and d15N in Beihai, Sanya, Xisha Islands and Nansha Islands. Therefore, the biomagnification of MeHg, measured by the Log10 (MeHg)-d15N slope, in marine fish from the South China Sea was location-specific. Tropic levels were estimated at Shantou, Pearl River Estuary and Sanya, where herbivorous fish S. canaliculatus was assigned a TL of 2 (Table 1). No significant difference in trophic level was observed between the locations (one-way ANOVA). Biomagnification of MeHg has been attributed to high dietary uptake efficiencies and slow elimination kinetics (Luoma and Rainbow, 2005). The dietary assimilation efficiencies (AEs) of MeHg were 90–91% for Terapon jarbua and juvenile blackhead seabream A. schlegeli (Dang and Wang, 2010, 2012). Moreover, it was estimated that over 90% of THg enters wild fish through their diet,

Log MeHg concentration (μg/g)

442

0.5 0.0 -0.5 -1.0 -1.5 -2.0 6

8

10

12

14

16

18

20

22

15

δ N (‰ ) Shantou y=0.189x-3.420 Pearl River Estuary y= -0.062x-0.168 Beihai y=-0.029x-0.527 Sanya y=0.252x-3.834 Xisha Islands y=0.097x-2.132 Nansha Islands y=0.576x-6.053 Fig. 2. Relationships between log-transformed MeHg concentration (lg/g dry wt) and d15N (‰) for different marine fish species inhabiting various parts of the South China Sea.

with higher accumulation rates in fish occupying the highest positions in the trophic chain (Wiener et al., 2003). Thus, the Log10 MeHg variability may also be explained using d15N in food web. Senn et al. (2010) reported that in six coastal species and two oceanic species, trophic position as measured by d15N explained most of the variance in Log10 MeHg. Campbell et al. (2005) found that Hg was biomagnified along the Northwater Polynya food web based on the significant positive relationship found between Log10 Hg concentration and d15N in fish muscles. Campbell et al. (2004) found a significant relationship between Log10 (THg) and d15N for fish from Thruston Bay, Lake Victoria. However, no significant biomagnification was found in the Pearl River Estuary, Beihai, Sanya, Xisha Islands and Nansha Islands. Biomagnification tends not to occur in areas where fish have similar d15N values and highly variable MeHg concentrations (Al-Reasi et al., 2007). On the other hand, the slopes of the regression of log-transformed MeHg concentration against d15N value were calculated to be 0.10 for Xisha Islands, 0.19 for Shantou and 0.25 for Sanya (Fig. 2). These slopes were comparable to the ones calculated for a tropical marine system, the oceanic food web in the Northern Gulf of Mexico, the marine food webs in eastern Canada and the contaminated estuarine food web in the Aveiro Lagoon of Portugal (Table 4). The Pearl River Estuary and Beihai showed negative

Table 3 Significant regression between fish muscle MeHg concentration and fish size (length and weight) of each species from different locations (p < 0.05, n > 5). Location

Species

Regression equation Length

Weight

Shantou

Pardachirus pavoninus Trypauchen vagina Nemipterus virgatus Johnius belangerii Trichiurus sp. Sillago sihama

y = 0.056x  0.429 (r = 0.80, p = 0.006) y = 0.043x  0.404 (r = 0.71, p = 0.009) y = 0.229x  3.756 (r = 0.84, p = 0.04) y = 0.036x  0.228 (r = 0.62, p < 0.0001) y = 0.069x  0.738 (r = 0.51, p = 0.004) y = 0.046x + 0.550 (r = 0.61, p = 0.05)

y = 0.006x  0.015 (r = 0.82, p = 0.003) – y = 0.011x  1.026 (r = 0.96, p = 0.002) y = 0.004x + 0.021 (r = 0.69, p < 0.0001) – –

Pearl River Estuary

Coilia mystus Mugil cephalus

y = 0.014x  0.093 (r = 0.67, p = 0.009) y = 0.014x  0.053 (r = 0.76, p = 0.004)

– y = 0.002x + 0.052 (r = 0.76, p = 0.004)

Beihai

Branchiostegus argentatus Trichiurus sp.

y = 0.014x  0.085 (r = 0.65, p = 0.0004) y = 0.013x  0.100 (r = 0.68, p < 0.0001)

y = 0.001x + 0.055 (r = 0.71, p < 0.0001) y = 0.001x + 0.056 (r = 0.72, p < 0.0001)

Sanya

Terapon theraps Polydactylus sextarius Nemipterus virgatus

y = 0.177x  1.735 (r = 0.79, p = 0.004) y = 0.086x  0.893 (r = 0.75, p = 0.005) y = 0.031x  0.142 (r = 0.81, p = 0.02)

y = 0.011x  0.085 (r = 0.71, p = 0.02) y = 0.007x  0.098 (r = 0.68, p = 0.01) y = 0.004x + 0.074 (r = 0.84, p = 0.009)

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A. Zhu et al. / Marine Pollution Bulletin 77 (2013) 437–444 Table 4 Slopes and trophic magnification factors (TMFs) between log transformed MeHg concentrations and d15N for different marine ecosystems. Location

Slop (d15N)

TMF

References

Arctic Tropical (Gulf of Oman) Arctic Gulf of St. Lawrence (Canada) Northern Gulf of Mexico

0.22 0.14 0.34 0.20 0.19 (oceanic) 0.28 (coastal) 0.26 0.14–0.31 0.19

1.66 1.38 2.19 1.58 1.55 (oceanic) 1.91 (coastal) 1.82 1.38–2.04 1.54

Campbell et al. (2005) Al-Reasi et al. (2007) Rigét et al. (2007) Lavoie et al. (2010) Senn et al. (2010)

Temperate estuarine (Portugal) Canada Subtropical (Shantou, China)

slopes of 0.06 and 0.03, respectively. To some extent, the negative slopes may be due to the fact that only fish communities were included in the calculations, whereas organisms at the lower trophic levels such as phytoplankton, zooplankton, and invertebrates, and predators at higher trophic levels such as sea birds and marine mammals were ignored. The TMF value of 1.54 for Shantou, where a significant relationship between Log10 (MeHg) and d15N was found, was similar to that observed in the Arctic, Baltic Sea, tropical lake Tanganyika and temperate Ria de Aveira estuary (Table 4). Since Shantou is a subtropical area, TMF values may show some degrees of stability regardless of latitudes, as suggested by van der Velden et al. (2013) and Coelho et al. (2013). In the present study, MeHg concentrations in a large number of marine fish species inhabiting various parts (some relatively far away from the coastline) of the South China Sea were quantified. Variability in MeHg concentrations in marine wild fish were related to differences in length, wet weight, feeding habit, habitat and trophic level. Carnivorous fish were found to possess the highest concentrations of MeHg, followed by planktivorous fish and herbivorous fish. The d15N of fish may be a predictor of tissue MeHg concentrations only for specific sites. There was a possible linkage between Hg concentrations in marine fish and Hg emissions from the surrounding inland areas. The present study indicates that fish from the South China Sea were generally not contaminated by Hg. Acknowledgements This study was supported by Open Project of Key Laboratory of Marine Bio-resources Sustainable Utilization (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences (LMB 091010) to Aijia Zhu, and a General Research Fund from the Hong Kong Research Grants Council (663112). References Al-Reasi, H.A., Ababneh, F.A., Lean, D.R., 2007. Evaluating mercury biomagnification in fish from a tropical marine environment using stable isotopes (delta C-13 and delta N-15). Environ. Toxicol. Chem. 26, 1572–1581. Amlund, H., Lundebye, A.K., Berntssen, M.H.G., 2007. Accumulation and elimination of methylmercury in Atlantic cod (Gadus morhua L.) following dietary exposure. Aquat. Toxicol. 83, 323–330. Anon., 2007. The Madison declaration on mercury pollution. Ambio 36, 62–65. Bank, M.S., Chesney, E., Shine, J.P., Maage, A., Senn, D.B., 2007. Mercury bioaccumulation and trophic transfer in sympatric snapper species from the Gulf of Mexico. Ecol. Appl. 17, 2100–2110. Burger, J., Gochfeld, M., 2006. Mercury in fish available in supermarkets in Illinois: are there regional differences. Sci. Total Environ. 367, 1010–1016. Campbell, L.M., Balirwa, J.S., Dixon, D.G., Hecky, R.E., 2004. Biomagnification of mercury in fish from Thruston Bay, Napoleon Gulf, Lake Victoria (East Africa). Afr. J. Aquat. Sci. 29, 91–96. Campbell, L.M., Norstrom, R.J., Hobson, K.A., Muir, D.C.G., Backus, S., Fisk, A.T., 2005. Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci. Total Environ. 351, 247–263. Chen, Z.Z., Qiu, Y.S., 2003. Estimation of growth and mortality parameters of Parargyrops edita Tanaka in Beibu Bay. J. Fish. China 27, 251–257 (in Chinese). Chen, H.M., Zheng, C.R., Tu, C., Zhu, Y.G., 1999. Heavy metal pollution in soils in China: status and countermeasures. Ambio 28, 130–134.

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