Environmental concentrations and bioaccumulations of cadmium and zinc in coastal watersheds along the Chinese Northern Bohai and Yellow Seas

Authors


Abstract

Cadmium (Cd) and zinc (Zn) in surface water, sediment, carp, and crab samples collected from upstream and downstream regions of coastal watersheds along the Chinese Northern Bohai and Yellow Seas were analyzed to provide a comprehensive understanding and assessment of their environmental concentrations and bioaccumulations. The results showed that downstream waters contaminated with Zn would have adverse effects on aquatic organisms. Although nearly all sediments were contaminated with Cd due to human activities, little potential existed for Cd toxicity in sediment-dwelling fauna. Concentrations of Cd and Zn in most water, sediment, carp, and crab were less than published values. The downstream carp and crabs had higher mean bioaccumulation factors and biota-sediment accumulation factors for Cd but lower mean biota-sediment accumulation factors for Zn than the upstream carp and crabs. Based on the relationships among Cd and Zn concentrations in water, sediment, and biota, the authors conclude that Cd and Zn in crabs primarily derived from sediment exposure. Although Cd and Zn in water and sediment originated from some of the same sources, the sources of Cd or Zn in water were likely different from those in sediment. Environ. Toxicol. Chem. 2013;32:831–840. © 2013 SETAC

INTRODUCTION

During the past several decades, pollution in coastal environments of China has become an increasingly serious threat. In particular, metals and metalloids such as cadmium (Cd), zinc (Zn), arsenic (As), and lead (Pb) have become major pollutants along China's coastal zone. As a consequence, water and sediment qualities in coastal watersheds have declined markedly, affecting the health of aquatic ecosystems and possibly humans through consumption of contaminated seafood 1. The safety of seafood has been compromised by the presence of metals, constituting a health risk for those who eat foods from these affected coastal areas 2.

The Bohai and Yellow Seas in North China, around which are positioned important economic development zones and large harbors, are located in the northern Pacific Ocean. The coastal areas of the Bohai and Yellow Seas contain some extensive industrial areas in which both large- and middle-scale enterprises are situated. These industries, including metallurgy, petroleum refining, and chemical production, are frequently situated near harbors. In addition, agriculture and mining create potential sources of metals in the coastal river watercourses along the Bohai and Yellow Seas. Considerable metal quantities are released through human activities and are transported to the coast and bays in the form of sewage effluents, industrial discharges, urban and agricultural runoff, atmospheric fallout, and deposits that are released farther upriver 3. Since the 1990s, concentrations of metals and metalloids in water and sediments have exceeded the water quality standards in some coastal areas 4–6.

Based on the results of previous studies, most metals entering the Bohai and Yellow Seas originate from the more northern regions in the vicinity of Liaodong Bay 7, 8. Due to their concentrations and toxicities, Cd and Zn have been identified as the two metals of greatest concern in the area 1, 9–11. Cadmium and zinc loadings that exceed natural background pose a potential problem for aquatic ecosystems and for humans 12. The issue of contamination by these two metals is especially critical for coastal areas in which riverine and land-based inputs discharge into a semi-enclosed embayment, as in the Chinese Northern Bohai and Yellow Seas. For this reason, significant quantities of Cd and Zn are trapped within the catchments.

Most previous studies conducted in the area have focused on Cd and Zn in water 3, 13 and sediment 4, 5, 8, 14, 15. However, only sporadic studies have extended beyond water and sediment to include biota 1, 16. Dietary metal uptake by aquatic organisms is known to be as important as waterborne metal uptake, and the relative importance of uptake from the water versus uptake from the diet depends on the metal, its bioavailable concentrations in water and diet, the habitat and feeding habits of the organism, and finally the uptake rate, assimilation efficiency, and detoxification/homeostatic processes in the organism. Therefore, in addition to measuring concentrations of metals in abiotic matrices, monitoring their bioaccumulation in aquatic animals is important to fully assess the potential impact on organism and human health 17. Bioaccumulation of Cd and Zn in aquatic foods is a potential problem from a public health standpoint. Furthermore, serious concerns have arisen in Chinese food safety, which also require knowledge of the bioaccumulated concentrations of Cd and Zn and their potential risks to humans. However, in China, integrated assessments of the concentration distributions of Cd and Zn in various matrices within the coastal watersheds on a regional scale and their bioaccumulations in the muscle tissue of aquatic foods such as carp and crabs are limited. In addition, the relative importance of local- versus watershed-scale effects on concentrations of metals along the Chinese Northern Bohai and Yellow Seas had not yet been determined. Currently, the potential for Cd and Zn in upstream areas of the watersheds, including surface waters, is largely unknown, specifically in freshwater systems that influence the metal concentrations when transported to downstream areas, such as coastal and estuarine systems and in particular marine and brackish systems. Therefore, a systematic study was needed to evaluate Cd and Zn in abiotic and biotic matrices from upstream and downstream regions of coastal watersheds along the Chinese Northern Bohai and Yellow Seas.

The specific objectives of the present study were (1) to determine concentrations of Cd and Zn in water and sediment and to assess their bioaccumulation by measuring their concentrations in carp and crabs; (2) to characterize the spatial distribution of Cd and Zn concentrations in water, sediment, and human food of aquatic origin; (3) to ascertain sources and relationships of Cd and Zn in surface water, sediment, and foods of aquatic origin; and (4) to evaluate the potential hazards of these two metals to wildlife and humans.

MATERIALS AND METHODS

Study area

A map of the study area and sample details of all sampling sites along the Chinese Northern Bohai and Yellow Seas are provided in Figure 1 and the Supplemental Data, Table S1, respectively. Two receiving waters for the coastal rivers exist along the Chinese Northern Bohai and Yellow Seas. One is the Northern Bohai Sea, which collects water from rivers to the west of Dalian. The other is the Northern Yellow Sea, which collects water from rivers to the east of Dalian. The Liugu, Wuli, Daling, Liaohe, Daliao, Daqing, and Fuzhou rivers flow north to south into the Northern Bohai Sea, while the other rivers flow north to south into the Northern Yellow Sea (Fig. 1). Approximately 28 million people live in the coastal watersheds along the Chinese Northern Bohai and Yellow Seas, with the watersheds in Tangshan having the largest population. The coastal watersheds in Jinzhou and Panjin contain the largest proportion of farmland. The largest proportions of urban and industrial areas are found in the watersheds in Tangshan and Dalian, where the largest quantities of industrial waste and sewage are discharged.

Figure 1.

Sampling sites for surface water, sediment, and aquatic food samples in upstream and downstream regions of the coastal watersheds (with a different shade representing a different administrative region) along the Chinese Northern Bohai and Yellow Seas. [Color figure can be seen in the online version of this article, available at wileyonlinelibrary.com]

Sampling

Our research group had previously chosen 36 sites, selected by simple random sampling to represent the typical characteristics of industry, agriculture, and urbanization along coastal watersheds of the Chinese Northern Bohai and Yellow Seas. A nested sampling scheme was applied to each site. All samples were collected in October 2008 (Fig. 1).

Thirty-six surface-water samples were collected (Supplemental Data, Table S1). Clean sampling techniques were used during sample collection, preservation, and storage 18. Twenty-one water samples were obtained from upstream regions of the rivers, and 15 were collected from downstream regions. Each water sample consisted of five homogenized subsamples (1 L) taken from 0- to 10-cm depths within an area of approximately 25 m2. These subsamples were then placed into precleaned and labeled Teflon bottles. To keep the dissolved metals in solution, the water samples were filtered through a 0.45-µm capsule filter and acidified with HNO3 to a pH of ≤2 at the time of collection. Samples were then placed in a cooler and immediately delivered to the laboratory.

Except for one location, surface sediments were collected synoptically with water. Thirty-five sediment samples were collected, of which 21 were from the upstream areas and 14 were from the downstream areas (Fig. 1). Each sediment sample was composed of five homogenized subsamples taken from the top 10 cm within a 5-m2 area. Composite sediment samples were placed in dark-colored Teflon bottles, refrigerated, and returned immediately to the laboratory where they were air-dried, crushed, mixed thoroughly, passed through a 100-mesh nylon sieve, and stored at 4°C in the dark prior to analysis.

Crucian carp (Carassius carassius) and Asian shore crabs (Hemigrapsus sanguineus) were selected as representative aquatic foods because their habitats are evenly distributed throughout the coastal areas along the Chinese Northern Bohai and Yellow Seas. To remove effects of specimen size within the same species, only individuals of approximately the same size were collected. Crucian carp with a length of 9 ± 2 cm (mean ± standard deviation [SD]) and a wet weight of 180 ± 30 g (mean ± SD) (estimated average age, 1–2 years) and Asian shore crabs with a carapace width of 3.2 ± 0.40 cm (mean ± SD) and a wet weight of 20 ± 3 g (mean ± SD; estimated average age 1–2 years) were collected. A composite sample of carp or crab contained three individuals that together formed a representative sample for each sampling site. Forty-one composite samples were collected. Ten of the 17 composite carp samples were from the upstream regions, and seven were from downstream regions. Six of the 24 composite crab samples were from upstream regions, and 18 were from downstream regions (Fig. 1 and Supplemental Data, Table S1). The biota samples were placed in watertight polyethylene bags and frozen at –20°C. In the laboratory, the samples were dissected, and equal weights of muscle from each replicate of the same species from each site were combined. The muscle aliquots were dried at 105°C for 24 h.

Quantification of heavy metals

The surface waters were analyzed directly. The sediments were digested using HNO3 and H2O2 according to U.S. Environmental Protection Agency method 3051 19. The aliquots of 0.10 to 0.45 g of dried muscle were homogenized, weighed, and digested in Teflon bombs using HNO3, H2O2, and HCl 20. Concentrations of Cd, Zn, and iron (Fe) in the digestates and reagent blanks were quantified via inductively coupled plasma-mass spectrometry (Agilent 7500; Agilent Technologies, Palo Alto, CA, USA).

Quality assurance and quality control for the quantification of heavy metals were determined by analyzing duplicates, method blanks, liquid standard solutions, and the certified reference materials GB ESS1 and DORM-2 for the sediment and biota samples, respectively. The limits of quantification for Cd and Zn were 0.07 and 1 µg/L, respectively. Concentrations of Cd and Zn in all method blanks were less than limits of quantification. Recoveries of Cd spiked in water, sediment, and biota were 99 ± 1, 98 ± 4, and 94 ± 2%, respectively, while recoveries of Zn spiked in water, sediment and biota were 101 ± 2, 97 ± 3, and 91 ± 5%, respectively. Recoveries of Fe from the sediment and biota were 101 ± 4 and 104 ± 3%, respectively. The relative percentage of difference between the sample duplicates was <10%.

Enrichment factor, bioaccumulation factor, and biota-sediment accumulation factor

Enrichment factors (EFs) were used to determine potential sources of metals into riverine, estuarine, and coastal environments 21. To identify anomalous metal concentrations, a geochemical normalization of Cd and Zn concentrations to concentrations of a conservative element, such as aluminum (Al), Fe, or silicon (Si), was employed. Several authors have successfully used iron to normalize the concentrations of metal contaminants 22. In the present study, Fe was used as the conservative tracer to differentiate the natural from the anthropogenic sources of Cd and Zn. The EF for each metal was calculated using the following Equation 1 23

equation image(1)

in which EF is the enrichment factor, equation image is the ratio of the concentrations of either Cd or Zn to Fe in the sample, and equation image is the ratio of the metal to the Fe concentration in the background. Considering the regional differences in Fe concentrations in sediment and the lack of data regarding the background concentrations of Fe in riverine sediment of China, the soil background Fe concentrations (mean = 28,800 mg/kg, dry wt, with a range of 11,200–46,400 mg/kg, dry wt) in the Liaoning Province where most coastal rivers along the Chinese Northern Bohai and Yellow Seas are located, and the sediment background Fe concentrations (mean = 34,800 mg/kg, dry wt, with a range of 7,300–51,500 mg/kg, dry wt) in the Bohai Sea were adopted as background values for the riverine and marine sediments in the studied area, respectively 24, 25.

Enrichment factor values between 0.5 and 1.5 indicated that the metal originated entirely from crustal materials or natural processes, whereas EF values greater than 1.5 suggested that the metal was more likely the result of human activities 26. Categories of contamination have been defined based on EF values. For example, EF values ≤ 2 suggest a deficiency in minimal metal enrichment. Alternatively, an EF value > 2 suggests various degrees of metal enrichment due to human activities 27.

The bioaccumulation factor (BAF) is the ratio of a chemical concentration in an organism to the concentration in water. The biota-sediment accumulation factor (BSAF) is the ratio of a chemical concentration in an organism to the concentration in sediment 28. Concentrations of Cd and Zn in muscle of carp and crabs in the present study were expressed on a wet-weight basis. These concentrations could be converted to a dry-weight basis by use of a wet-to-dry-weight conversion factor 29. In the present study, the wet-to-dry conversion factors for carp and crabs were 4.2 ± 0.67 and 3.4 ± 1.0, respectively.

Data analysis

Concentrations of Cd and Zn in water, sediment, carp, and crabs as well as EFs, BAFs, and BSAFs were logarithmically transformed to better approximate the normal distributions of the values. The Shapiro–Wilk test was used to test for normality. The t test for independent groups was used to determine whether the concentrations of metals in water, sediment, carp, and crabs as well as EFs, BAFs, and BSAFs for the upstream coastal watersheds differed significantly from those for the downstream coastal watersheds. Correlations between the metal concentrations in abiotic and biotic materials were also performed. Pearson correlation coefficients (r) were calculated for several pairs of variables. The significance level (α) was set at 0.05. All statistical analyses were conducted using SPSS version 16.0.

RESULTS

Cadmium and zinc concentrations in the water samples from the upstream and downstream sites of the coastal watersheds along the Chinese Northern Bohai and Yellow Seas are presented in Table 1. In general, mean concentrations of Cd and Zn in downstream waters within coastal watersheds along the Chinese Northern Bohai and Yellow Seas were significantly higher than those in the upstream waters (p < 0.01). No differences were found in mean concentrations of Cd and Zn in upstream waters between the Northern Bohai Sea and Northern Yellow Sea (p > 0.05). However, mean concentrations of Cd and Zn in the downstream waters of coastal rivers along the Northern Bohai Sea were greater than those in downstream waters of the coastal rivers along the Northern Yellow Sea (p < 0.05; Table 1). Water from upstream in the Yalu River contained the highest Zn concentration, while water from downstream in the Wuli River contained the highest Cd concentration (Fig. 2). Relatively high Cd and Zn concentrations in downstream waters were predominantly distributed around the Northern Bohai Sea, especially around Liaodong Bay. The levels of Cd in water of the Dou and Luan rivers, in seawater of Jinzhou and Liaodong Bays, in the Yalu River Estuary, and even in the Northern Bohai Sea can be considered small, compared to previous studies of Cd and Zn in these regions (Supplemental Data, Table S2), while Cd levels in the seawater of the Daliao Estuary and the Northern Yellow Sea can be considered high in comparison with previous studies. The mean Zn concentrations in the seawater of the Northern Bohai Sea and Northern Yellow Sea in the present study showed a slight increase, while those from the Daliao River Estuary, Jinzhou Bay, and the Liaodong Bay showed a large decrease (Fig. 2 and Supplemental Data, Table S2).

Table 1. Cadmium (Cd) and zinc (Zn) concentrations in water (µg/L), sediments (mg/kg, dry wt), and their enrichment factor (EF) values in the coastal watersheds along the Chinese Northern Bohai and Yellow Seas (CNBYS)
Environmental sampleSampling locationStatisticCdZn
  1. GM = geometic mean; SD = standard deviation; NBS = Northern Bohai Sea; NYS = Northern Yellow Sea.

WaterUpstream regions of coastal watersheds along the NBS (n = 17)GM ± SD0.20 ± 0.0317.0 ± 4.52
Downstream regions of coastal watersheds along the NBS (n = 12)GM ± SD0.37 ± 0.1822 ± 10
Upstream regions of coastal watersheds along the NYS (n = 14)GM ± SD0.19 ± 0.00119.7 ± 59
Downstream regions of coastal watersheds along the NYS (n = 3)GM ± SD0.28 ± 0.1013 ± 29
Upstream regions of coastal watersheds along the CNBYS (n = 21)GM ± SD0.20 ± 0.0317.5 ± 26
Downstream regions of coastal watersheds along the CNBYS (n = 15)GM ± SD0.35 ± 0.1720 ± 14
SedimentUpstream regions of coastal watersheds along the NBS (n = 17)GM ± SD0.13 ± 0.1850 ± 39
EF ± SD2.2 ± 2.01.5 ± 0.82
Downstream regions of coastal watersheds along the NBS (n = 12)GM ± SD0.11 ± 0.08234 ± 33
EF ± SD5.0 ± 2.51.8 ± 0.76
Upstream regions of coastal watersheds along the NYS (n = 4)GM ± SD0.13 ± 0.07186 ± 44
EF ± SD1.4 ± 0.311.8 ± 0.47
Downstream regions of coastal watersheds along the NYS (n = 2)GM ± SD0.10 ± 0.06290 ± 0.87
EF ± SD1.3 ± 0.672.0 ± 0.63
Upstream regions of coastal watersheds along the CNBYS (n = 21)GM ± SD0.13 ± 0.1667 ± 41
EF ± SD2.0 ± 1.81.6 ± 0.76
Downstream regions of coastal watersheds along the CNBYS (n = 14)GM ± SD0.11 ± 0.08149 ± 34
 EF ± SD4.7 ± 2.61.8 ± 0.73
Figure 2.

Spatial distribution of Cd and Zn in water (A) and sediment (B) from upstream and downstream regions of the coastal watersheds along the Chinese Northern Bohai and Yellow Seas. [Color figure can be seen in the online version of this article, available at wileyonlinelibrary.com]

Mean concentrations of Cd and Zn in upstream and downstream sediments of coastal watersheds along the Chinese Northern Bohai and Yellow Seas are provided in Table 1. Mean concentrations of Cd and Zn in upstream sediments were not significantly greater than those in downstream sediments (p > 0.05). Mean concentrations of Zn in the up- and downstream sediments that were collected from coastal watersheds along the Northern Yellow Sea were greater than those from coastal watersheds along the Northern Bohai Sea (p < 0.05). However, no differences were observed in mean Cd concentrations in the up- and downstream sediments between the Northern Bohai Sea and Northern Yellow Sea (p > 0.05; Table 1). Sediments in both the up- and downstream areas of rivers such as the Wuli, Yalu, and Yingna contained relatively high concentrations of Cd and Zn (Fig. 2). Mean EF values for Cd and Zn in sediments were greater than 1.5. Mean EFs for Zn were less than 2 (EF < 2) in both upstream and downstream sediments. The mean EF value for the Cd concentration in the downstream sediments was greater than that in upstream sediments (p < 0.05). However, the mean EF for Zn in upstream sediments did not differ significantly from that in downstream sediments (p > 0.05; Table 1). When these results were compared with those in the literature (Supplemental Data, Table S2), it was determined that (1) Cd concentrations in the sediments of Liaodong Bay in the present study are comparable, while those in other sediments are less (Fig. 2); (2) concentrations of Cd and Zn in upstream sediments of the Wuli, Liao, and Daliao rivers in the present study decreased greatly; and (3) the estuaries around Liaodong Bay (not including the Daliao Estuary), the Yalu Estuary, Jinzhou Bay, and Liaodong Bay had low concentrations of Zn; however, the mean Zn concentration in the downstream sediments of the Northern Yellow Sea was higher than that previously reported (Supplemental Data, Table S2).

Mean concentrations of Cd and Zn in muscles of carp are provided in Table 2. The mean concentration of Zn in upstream carp was significantly higher than that in downstream carp (p < 0.01), while no significant difference was found in mean concentrations of Cd in upstream and downstream carp (p > 0.05). Although carp from upstream portions of watersheds of the Northern Bohai Sea contained a greater mean Zn concentration than carp from upstream regions of watersheds of the Northern Yellow Sea (p < 0.05), no differences were detected in mean concentrations of Cd and Zn in carp between the Northern Bohai Sea and Northern Yellow Sea (p > 0.05). Carp from upstream areas of the Dou River in Tangshan and downstream areas of the Xin River in Qinghuangdao contained the highest Cd concentrations (Fig. 3). Higher Zn concentrations were observed in carp from the upstream areas of the Dou, Xin, Liugu,Wuli, and Fuzhou rivers. For the Northern Bohai Sea and Northern Yellow Sea, the mean BAFs and BSAFs for Cd in downstream carp were higher than those in upstream carp (p < 0.05; Table 2). Furthermore, the mean BAFs for Cd in upstream or downstream carp from the Northern Yellow Sea were higher than those from the Northern Bohai Sea. However, mean BSAF for Cd in upstream carp from the Northern Yellow Sea was less than that from the Northern Bohai Sea, while the mean BSAF for Cd in downstream carp from the Northern Yellow Sea was higher than that from the Northern Bohai Sea. For the Northern Bohai Sea and Northern Yellow Sea, mean BAFs and BSAFs for Zn were less in the downstream carp than in upstream carp. Furthermore, both BAF and BSAF for Zn in upstream carp from the Northern Bohai Sea were higher than those in upstream carp from the Northern Yellow Sea. However, the mean BAF for Zn was less in downstream carp from the Northern Bohai Sea than in downstream carp from the Northern Yellow Sea, while the mean BSAF for Zn was higher in downstream carp from the Northern Bohai Sea than in downstream carp from the Northern Yellow Sea. No studies could be found in the literature regarding concentrations of Cd and Zn in carp or other river fish in the studied areas. Therefore, we compared our results with data for sea fish species (Supplemental Data, Table S2). All Cd concentrations in carp were significantly less than previously reported concentrations of Cd in muscle of sea fishes. The Zn concentration in the carp from the sea near Huludao was remarkably lower than that previously reported for pomfret, blue-spot sierra, and gobies. Furthermore, carp from downstream in the Liao River in the present study had less concentrations of Zn than the wolf goby previously collected from the Liao River Estuary. However, the carp from the Northern Yellow Sea had a higher concentration of Zn than the fish previously collected from the Yellow Sea (Fig. 3, Supplemental Data, Table S2).

Table 2. Cadmium (Cd) and zinc (Zn) concentrations (mg/kg, wet wt), their bioaccumulation factors (BAFs), and bio-sediment accumulation factors (BSAFs) in carp and crab collected from the coastal watersheds along the Chinese Northern Bohai and Yellow Seas (CNBYS)
BiotaSampling locationStatisticCdZn
  1. GM = geometric mean; SD = standard deviation; NYS = Northern Yellow Sea; NBS = Northern Bohai Sea; NBYS = Northern Bohai and Yellow Seas.

CarpUpstream regions of coastal watersheds along the NBS (n = 8)GM ± SD0.0036 ± 0.04238 ± 15
BAF ± SD90.7 ± 224.69,042.0 ± 12211
BSAF ± SD0.26 ± 0.671.0 ± 0.86
Downstream regions of coastal watersheds along the NBS (n = 5)GM ± SD0.020 ± 0.1010 ± 6.7
BAF ± SD168.1 ± 295.4536.3 ± 335.1
BSAF ± SD1.0 ± 1.60.54 ± 0.54
Upstream regions of coastal watersheds along the NYS (n = 2)GM ± SD0.0026 ± 0.0004214 ± 0.26
BAF ± SD140.0 ± 368.62,454.2 ± 30,118.2
BSAF ± SD0.17 ± 0.540.24 ± 0.20
Downstream regions of coastal watersheds along the NYS (n = 2)GM ± SD0.01 ± 0.1119 ± 0.69
BAF ± SD245.4 ± 361.51,516.6 ± 2,567.1
BSAF ± SD2.3 ± 3.60.22 ± 0.31
Upstream regions of coastal watersheds along the NBYS (n = 10)GM ± SD0.0044 ± 0.0439 ± 17
BAF ± SD95.6 ± 212.38,383.2 ± 11,699.7
BSAF ± SD0.25 ± 0.630.85 ± 0.69
Downstream regions of coastal watersheds along the NBYS (n = 7)GM ± SD0.018 ± 0.0914 ± 6.4
BAF ± SD190.2 ± 294.7816.4 ± 934.6
BSAF ± SD1.2 ± 1.50.48 ± 0.50
CrabUpstream regions of coastal watersheds along the NBS (n = 6)GM ± SD0.14 ± 2.527 ± 6.7
BAF ± SD3,451.8 ± 7,448.71,842.2 ± 1,714.5
BSAF ± SD7.3 ± 15.71.2 ± 1.1
Downstream regions of coastal watersheds along the NBS (n = 18)GM ± SD1.6 ± 4.731 ± 12
BAF ± SD9,302.4 ± 12,008.21,496.8 ± 854.5
BSAF ± SD23.7 ± 21.20.64 ± 0.35
Downstream regions of coastal watersheds along the NYS (n = 4)GM ± SD0.29 ± 1.844 ± 9.1
BAF ± SD4,877.8 ± 5,427.56,180.4 ± 1,263.2
BSAF ± SD23.3 ± 25.90.49 ± 0.11
Upstream regions of coastal watersheds along the NBYS (n = 6)GM ± SD0.14 ± 2.527 ± 6.7
BAF ± SD3,451.8 ± 7,448.71,842.2 ± 1,714.5
BSAF ± SD7.3 ± 15.71.2 ± 1.1
Downstream regions of coastal watersheds along the NBYS (n = 22)GM ± SD1.2 ± 3.835 ± 12
BAF ± SD8,497.9 ± 11,135.12,348.3 ± 2,058.6
BSAF ± SD23.6 ± 21.50.61 ± 0.32
Figure 3.

Spatial distribution of Cd and Zn in carp (A) and crabs (B) from the coastal watersheds along the Chinese Northern Bohai and Yellow Seas. [Color figure can be seen in the online version of this article, available at wileyonlinelibrary.com]

Mean concentrations of Cd and Zn in the upstream crabs were significantly less than those in downstream crabs (p < 0.05; Table 2). No crabs were collected from the upstream areas within coastal watersheds along the Northern Yellow Sea. The mean Cd concentration in crabs from downstream regions of the coastal watersheds along the Northern Bohai Sea was greater than that in crabs from downstream regions of the coastal watersheds along the Northern Yellow Sea (p < 0.05), although no significant difference was detected in their Zn concentrations. Higher concentrations of Cd and Zn were primarily observed in crabs from upstream regions of the Xin and Daliao rivers and from downstream regions of the Wuli, Daliao, Daqing, Fuzhou, and Yingna rivers (Fig. 3). Mean BAF and BSAF for Cd were higher in downstream crabs than in upstream crabs. For the coastal watersheds along the Chinese Northern Bohai and Yellow Seas, the mean BAF for Zn was higher in downstream crabs than in upstream crabs, while the mean BSAF for Zn was lower in downstream crabs than in upstream crabs. We compared our results with the literature data of the studied areas (Supplemental Data, Table S2) and found that crabs from downstream in the Liao River had higher Cd concentrations (Fig. 3) than Orithyia sinica from the Liao River Estuary. Downstream crabs from Jinzhou Bay had Cd concentrations higher than previously reported for clams. However, downstream crabs from the sea near Huludao had Cd concentrations lower than previously reported for clams and mussels. The mean Cd concentration in downstream crabs from coastal watersheds along the Northern Yellow Sea was lower than previously reported concentration of Cd in crustaceans from the Yellow Sea. Zinc concentrations in carp from Jinzhou Bay were higher than those in clams and mussels previously collected from the same region. However, Zn concentrations in crabs from the Liao River Estuary and the sea near Huludao in the present study (Fig. 3) were significantly lower than those in clams and mussels collected in the same regions (Supplemental Data, Table S2).

To examine the relationships between Cd and Zn, in water, sediment, and biota (carp and crabs), a correlation table (Pearson correlation coefficients) was established (Table 3). Cadmium concentrations in crabs were significantly correlated with Cd and Zn concentrations in sediments (p < 0.05). Zinc concentrations in crabs had a significantly positive correlation with Zn in sediments (p < 0.05). Furthermore, Zn and Cd concentrations in crabs were significantly correlated with each other (p < 0.01). Cadmium concentrations in carp were not significantly correlated with Cd concentrations in water and sediments. Zinc concentrations in carp were negatively correlated with Cd concentrations in water (p < 0.01). Cadmium concentrations in carp were positively correlated with Zn concentrations in water and sediments (p < 0.01). Cadmium concentrations were significantly correlated with Zn concentrations not only in water but also in sediments. No significant correlations were observed between Cd or Zn concentrations in water and those in sediments.

Table 3. Correlation coefficients between concentrations of cadmium (Cd) and zinc (Zn) in water, sediment, and biota (number of samples in parentheses)
Pearson correlationCd-waterZn-waterCd-sedimentZn-sedimentCd-biotaaZn-biotaa
  • a

    Pearson coefficients for carp and crabs are shown above and below the diagonal line, respectively.

  • b

    Correlation is significant at the 0.05 level (two-tailed).

  • c

    Correlation is significant at the 0.01 level (two-tailed).

Cd-water10.52c (36)0.031 (35)–0.071 (35)0.11 (17)–0.65c (17)
Zn-water0.52c (36)10.07 0 (35)0.12 (35)0.13 (17)–0.44 (17)
Cd-sediment0.031 (35)0.070 (35)10.69c (35)–0.39 (17)–0.031 (17)
Zn-sediment−0.071 (35)0.12 (35)0.69c (35)10.011 (17)0.13 (17)
Cd-biotaa0.26 (28)0.33 (28)0.46b (28)0.50c (28)1–0.080(17)
Zn-biotaa0.19 (28)–0.20 (28)0.13 (28)0.38b (28)0.49c (28)1

DISCUSSION

Cadmium concentrations in waters from upstream were lower than the Chinese environmental quality standard for surface water (CEQSSW) Class I criterion (Supplemental Data, Table S3). The mean concentration of Zn in upstream waters was below the CEQSSW Class I criterion (Table 1 and Supplemental Data, Table S3). Except for one water sample taken from upstream in the Yalu River, which had a concentration of 123 µg Zn/L, all Zn concentrations were below the CEQSSW Class I criterion.

Cadmium concentrations in waters from downstream were lower than the Chinese sea water quality standard (CSWQS) Class I criterion (Supplemental Data, Table S3). However, 67% of concentrations of Zn in downstream waters, predominantly located near Qinghuangdao, Huludao, Panjin, and Dalian along Liaodong Bay of the Northern Bohai Sea, exceeded the CSWQS Class I criterion. Downstream water from Dalian (DL3) contained Zn concentrations that exceeded the CSWQS Class II criterion (Fig. 2 and Supplemental Data, Table S3). Therefore, most downstream waters from coastal sites along the Northern Bohai Sea were contaminated with Zn. Several zinc-related industries in addition to urbanization in Qinghuangdao, Huludao, Yinkou, and Dalian could be responsible for the Zn contamination in downstream water.

Based on the U.S. Environmental Protection Agency guidelines for maximum allowable acute and chronic values for Cd of 5.7 and 1.3 µg/L 30, and for Zn of 374 and 30 µg/L 31 in freshwater, respectively, none of the Cd concentrations observed in any river in the present study should produce potential toxic effects, but 17% of the water samples had Zn concentrations within the acute and chronic guidelines, which would indicate some adverse effects on aquatic organisms.

The mean Cd concentration in downstream sediments within the coastal watersheds was 73% higher than the background concentration in the marine sediments (95% confidence limits were 0.080–0.17 mg/kg, dry wt). However, mean Zn concentrations in both upstream and downstream sediments were less than the regional background concentration (Table 1 and Supplemental Data, Table S3).

Except for upstream sediments of the Wuli River, concentrations of Cd and Zn in nearly all sediments were less than the marine sediment quality Class I criteria (Fig. 2 and Supplemental Data, Table S3). Based on the threshold effect level, the effects range-low concentration and the probable effect level for Cd and Zn in sediment (Supplemental Data, Table S3), only 9% of sediments, located in the upstream regions of the Wuli and Yalu rivers, had Cd and Zn concentrations above the low-range values (threshold effect levels or effects range-low concentration; Fig. 2). Thus, only at these sites is there a possibility of toxicity from Cd and Zn in sediment-dwelling fauna.

Previous reports have indicated that ecosystems of the Wuli River have been significantly impacted by past and current loadings of Cd and Zn from certain industrial complexes such as the Huludao zinc plant (established in 1935) and the Jinzhou chemical refinery plant (established in 1937) 8, 32. Sediments of the Yalu River have been polluted with Cd and Zn discharged by copper mining, automobile manufacturing, paper making, dyeing, and textile industries in Dandong 14, 15. Furthermore, Cd and Zn can enter water and sediments from other industrial activities such as coal combustion, electroplating processes, iron and steel production, and pigment making, which occur along the Wuli and Yalu rivers. In addition, agricultural uses of phosphate fertilizers and sewage sludge and wastewater discharged from households in coastal cities may be identified as other sources of Cd and Zn to the water and sediments 4, 5, 8, 14, 15, 33.

All of the EF values for Cd and Zn in the sediments were greater than 1.5, indicating that the sources of Cd and Zn were likely due to human activity. Based on previously reported results 27, because mean EF values for Cd were greater than 2, Cd in up- and downstream sediments should be given more attention than Zn.

Three composite carp samples from the Dou and Biliu rivers and a coastal site in Qinghuangdao (Fig. 3) contained Cd concentrations greater than the quality standard set by the Ministry of Agriculture of China for the protection of human health (Supplemental Data, Table S3). Cadmium concentrations in other carp were below permitted concentration prescribed by the Food and Agriculture Organization. Carp from most watersheds were not contaminated with Cd. A total of 60% of the carp from upstream areas, primarily distributed around Liaodong Bay, had Zn concentrations higher than standard regulated by China. However, all downstream carp had Zn concentrations below this standard. Thus, most upstream carp contained sufficient Zn concentrations to be deemed unfit for human consumption.

The bioaccumulation factor provides an indication of accumulation efficiency of Cd and Zn in muscles of carp. The data in Table 2 clearly indicate that a high BAF for Cd was recorded in downstream carp while a high BAF for Zn was observed upstream carp. Zinc exhibited higher BAFs in the muscles of carp than Cd. Values of BSAF higher than 1 reveal that capacities of downstream carp to accumulate Cd and upstream carp to accumulate Zn are greater than those in sediments. In carp, the mechanism of bioaccumulation of Cd is different from that of Zn. This is likely because Zn is a required element and concentrations in tissues are homeostatically regulated 34.

Apart from one crab from the upstream region of the Daliao River (YK2) that contained the highest Cd concentration (6.3 mg/kg; Fig. 3), concentrations of Cd and Zn in crabs from other upstream areas were not only less than the limits prescribed by the Food and Agriculture Organization but were also less than the standards regulated by China (Supplemental Data, Table S3). However, approximately 70% of downstream crabs contained Cd concentrations higher than the concentration recommended by the Food and Agriculture Organization and China. Approximately 40% of downstream crabs contained Zn concentrations greater than the concentration prescribed by the Food and Agriculture Organization, but none of the Zn concentrations in crabs exceeded the limit established by China. It can, therefore, be concluded that muscle residues of Cd exceeded the guideline trigger values. Given that governmental guidelines for risk (to aquatic life and to human health) are very conservative, exceeding them could signify the potential for risks. In addition, Figure 3 shows that these crabs were primarily distributed around Liaodong Bay and in the central parts of coastal regions along the Northern Yellow Sea.

The BAFs and BSAFs for Cd indicate that elevated Cd concentrations in downstream crabs originate more from water and food than those in upstream crabs. There was variation of BAF and BSAF of Zn in crabs. The reason may be that Zn is an essential metal and has normal physiological regulatory functions, but can bioaccumulate and reach toxic levels 35. Concentrations of essential Zn in organisms tend to be highly regulated compared with nonessential metals such as Cd 34. Cadmium exhibited relatively higher BAFs and BSAFs than Zn in muscle of crabs. More attention should be given to bioaccumulated Cd in muscle of crabs, which can pose potential risks to humans. By comparing BAFs and BSAFs for Cd and Zn between carp and crabs, it can be concluded that carp has relatively high accumulation of Zn while crab has a relatively high accumulation of Cd. Most biotic factors that influence metal bioaccumulation are associated with diet and include metal concentrations in prey species and feeding rate. Therefore, future studies analyzing Cd and Zn in the most important food sources, as well as their uptake rates, assimilation efficiencies, and detoxification mechanisms by crabs, could yield more insights into the contribution of each pathway 36, 37.

The significantly positive correlation between concentrations of Cd in crabs and concentrations of Cd and Zn in sediments indicated that the relative abundance of Cd in crabs reflects an accumulation that is proportional to concentrations of Cd and Zn in sediments. The positive correlation between the Zn concentrations in crabs with Zn concentrations in sediments suggested that Zn concentrations increased in muscle of crabs as a result of indirect exposure through the food chain. Crabs are closely associated with surface sediments because they are bottom dwellers. Thus, Cd and Zn can be taken up indirectly by eating sediment-dwelling invertebrates. Similar results have been observed in bivalves; concentrations of metals in tissue are related to concentrations of metals in sediments 38. A strong positive association between concentrations of Zn and Cd in crabs implied that the Cd and Zn originated from a common source. Blackmore and Wang (2002) found the same results in green mussels 39. Positive relationships between the Cd and Zn in water and sediment implied that Cd and Zn had common sources in water and sediment. It has been shown that Cd is commonly found in association with Zn. Rather surprisingly, no significant correlations in Cd or Zn concentrations were found between water and sediment, suggesting that sources of Cd or Zn in water were likely to differ from those in sediment.

Based on varied environmental concentrations of Cd and Zn as well as biological characteristics in the fields, single EF, tissue concentration, BAF, or BSAF could not be used as an indicative of pollution sources or hazards posed by these metals. Therefore, different methods should be applied in the investigation of environmental concentrations of metals and their bioaccumulations in the future.

CONCLUSIONS

Mean concentrations of Cd and Zn in downstream waters were significantly greater than those in upstream waters within the coastal watersheds along the Chinese Northern Bohai and Yellow Seas. This fact was especially true for waters in the watersheds along the Northern Bohai Sea. Most downstream waters were contaminated by Zn. Apart from upstream areas of the Wuli and Yalu rivers, concentrations of Cd and Zn in sediments were not sufficient to cause adverse effects on the sediment-dwelling fauna. Cadmium and Zn were present in the highest concentrations in water and sediment of up- and downstream areas of the Liugu, Wuli, Daliao, and Yalu rivers. Based on measured enrichment factors, Cd contamination in all sediments is of concern. Mean Zn concentration in upstream carp was higher than that in downstream carp. Upstream carp from the Northern Bohai Sea had a greater mean concentration of Zn than upstream carp from the Northern Yellow Sea. The mean Cd concentration in downstream crabs from the coastal watersheds along the Northern Bohai Sea was greater than that in downstream crabs from the coastal watersheds along the Northern Yellow Sea. Concentrations of Cd and Zn in most waters and sediments were below the published values, indicating a recent improvement in water and sediment qualities. Compared to the literature, concentrations of Cd and Zn in most carp and crabs can be considered low. Downstream carp and crabs had higher mean BAFs and BSAFs for Cd than upstream carp and crabs, while upstream carp and crabs had higher BSAFs for Zn than downstream carp and crabs. Concentrations of Cd and Zn in crabs were significantly correlated with those in sediments, indicating that both the Cd and the Zn in the crabs originated from the sediments. Cadmium and Zn shared common sources in water and sediment. However, sources of Cd or Zn in water were likely to differ from those in sediment.

SUPPLEMENTAL DATA

Tables S1–S3. (215 KB DOC).

Acknowledgements

This research was supported by the National Natural Science Foundation of China under grants 41271502 and 41071355, Strategic Priority Research Program of the Chinese Academy of Sciences, Grant No. XDB03030504, the National International S&T Cooperation Program under grant 2012DFA91150, the Einstein Professorship Program, Chinese Academy of Sciences, and the Project of the State Key Lab of Urban and Regional Ecology under grant SKLURE2008-1-04. Portions of the research were supported by a Discovery Grant from the Natural Science and Engineering Research Council of Canada (Project 6807). We are grateful to two anonymous reviewers and the editor for their constructive comments and suggestions.

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