Arsenic concentrations in the habitat and the prey of the Red-Crowned Crane (i.e. reed rhizomes and three aquatic animal families [Perccottus glehni Dybowski, Cybister japonicus Sharp and Viviparidae]) were analyzed to examine the bioaccumulation of arsenic in Red-Crowned Cranes in northeastern China. The results indicated that arsenic concentrations in the prey of the Red-Crowned Cranes were elevated via food chain. Most of the detected arsenic contents in the sediments were below the natural background level (7.49 ppm) and ranged from 0.34 to 8.32 ppm (dry weight). The geo-accumulation indices at all sites were less than 0, which suggests the region had only background concentrations of arsenic. Three aquatic animal families were observed to contain some arsenic, with the following order of increasing concentrations: primary consumer < secondary consumers. The arsenic concentrations of sediments and water animals in the buffer zone were significantly higher than those in the core area, and increased in higher trophic level animals. The highest arsenic metal concentrations were found in the livers of the Red-Crowned Cranes (in a range of 145.46 ppb to 367.78 ppb) compared with the kidneys (116.44 ppb to 257.46 ppb) and muscles (63.45 ppb to 94.26 ppb). By contrast, the feathers had the lowest concentrations, with an average of 32.25 ppb. The dietary exposure level of arsenic to the Red-Crowned Crane population in Zhalong wetland of northeastern China appeared to be below arsenic toxicity threshold concentrations.

Introduction

Arsenic (As) is of primary concern regarding its health effects on waterfowl (Burger and Gochfeld, 1997), although it is a relatively common element that occurs in various organic and inorganic forms in the environment. Increasing evidence indicates that As is nutritionally essential or beneficial at low concentrations (Eisler, 1988; Abedin et al., 2002; Williams et al., 2007). With increasing concentration, As becomes toxic for the environment and living organisms by causing inhibition of growth (Gulz et al., 2005), liver and kidney damages, eventually causing death (Shaw et al., 2007). Aside from industrial activities such as coal combustion and glass manufacturing that release As into the environment (Eisler, 1988), the application of As-containing fertilizers and pesticides has led to a widespread As pollution in soils (Eisler, 1988). In aquatic environments, As tends to bind with particulate matter and is deposited into sediment (EPA, 1980). Some As would be readily taken up by aquatic plants (e.g. reed) or benthic-feeding organisms and can be found elevated in high stratum-level animals (Fisk et al., 2005; Agah, 2009). Therefore, the build-up of As concentrations in sediment and water bird should be determined to detect the net change in ecological systems.

Recent research have shown that the body burdens of metals in animals are proportional to the metal content in the environment (Martínez–Villegas et al., 2004; Burger et al., 2008; Fisk et al., 2005). Frequently, environmentally sensitive aquatic plants (i.e. reed) (Hansan et al., 2009), fish (Nsikak et al., 2007), and water birds are often employed to indicate the pollution levels of a metal-contaminated region (Fasola et al., 1998).

Red-Crowned Crane (Grus japonensis) is precious and in danger of extinction, as listed by the International Union for Conservation of Nature and Natural Resources (ICUN) Red List of Endangered Species since 2000 (BirdLife International, 2012). This species has a small worldwide population of 2,750 mature individuals; although their population in Japan (resident population) is stable (Teraoka et al., 2007), the mainland Asian population (migratory population) continues to decline because of the loss and degradation of wetlands through conversion to agriculture and industrial development (Harris, 2008). Red-Crowned Cranes are omnivores and typically feed on aquatic plants (e.g. reed root and stem) and water animals (e.g. fish, shell and aquatic insect). Prey may significantly contribute to the dietary intake of As for large water animals (Eisler, 1988). Red-Crowned Cranes often roost and nest at the same site in their life, which may cause eventual accumulation of As in their bodies if they are chronically exposed to contaminated habitat and prey (Koller, 1980).

Wuyur River originates from the western foot of Xiaoxin’an Mountain, northeastern China, wherein the watershed is an elongated strip and flows through the main food production zone of Heilongjian Province in China (Figure 1a). The lower reaches of the riverway are replaced by a large area of reed marsh after entering into the Zhalong National Nature Reserve (Zhalong wetland). Zhalong wetland covers an area of 2,100 km2 (123º51′ to 124º37′ E, 46º48′ to 47º32′N) (core area, which is the roosting and breeding site of endangered water birds, e.g. Red-Crowned Cranes, is approximately 700 km2; buffer zone occupies 1,400 km2 surrounding of the core area for protecting other common water birds) (Figure 1b). A large area of pristine reed marsh in the wetland attracts more than approximately 500 migratory Red-Crowned Cranes to inhabit and breed from late March to early November (approximately eight months) every year. River feeding and precipitation are the major sources of water in this inland reed marsh. Pesticides (e.g. lead arsenate and lead arsenate) and fertilizer contained As had been applied widely in the mid and late 20th century in the large area of arable land surrounding the wetland may contribute to As loadings in the wetland and to considerable As exposure to Cranes. However, no research has been conducted on the As-enrichment and dietary exposure in the migratory Red-Crowned Cranes in this region.

This research aims to examine the heavy metal enrichment levels in the prey of Red-Crowned Cranes and determine the exposure levels and compare them with the toxic dose of As for Red-Crowned Cranes. The present article is the first report on As accumulation and dietary exposure in the Red-Crowned Crane population in northeastern China, and the results from this research would improve our understanding of the ecological health safety of the migratory Red-Crowned Cranes in China.

Materials and methods

A total of 19 sampling sites were selected for sediment and aquatic plant (i.e. reed) collection. The first set of two sample sites (i.e. S1 and S2) were in the middle reaches of Wuyur catchments; the second set of ten sample sites (S3–S10, S15 and S16) were in the buffer zone A of the Zhalong marsh; the third set of six sample sites (i.e. S11–S14, S17 and S18) were in the core area of the wetland, and the remaining one sample (at S19) was selected in the buffer zone B of the wetland (Figure 1c). Surface sediment was collected with a sediment grab sampler, and packed in dark-colored polyethylene bags, refrigerated, and then transported back to the laboratory following the method by Abedin et al. (2002). The reed rhizome at each site was sampled simultaneously.

Three aquatic animal species, i.e. Perccottus glehni Dybowski (P. Dybowski), Cybister japonicus Sharp (C. Sharp) and Pond Snail (Viviparidae), which are typical preys of the Red-Crown Cranes in the wetland were collected from the selected sampling sites (P. Dybowski were trapped at S1—S19; C. Sharp were trapped at S4, S15, S16 and S17; Pond Snails were collected at S1–S15 and S17–S19). All of the prey samples were rinsed thoroughly in the field with distilled water to remove the pollutants attached on their body, then placed in a refrigerator at −4°C and transported back to the laboratory. Fish (P. Dybowski) were dissected into three sections, i.e. head section, intermediate section (mainly digestive function section) and tail (mainly excretory function section), Pond Snails were separated into two parts; i.e. soft body (slug) and shell; and C. Sharp were separated into two parts; i.e. head section and the remaining part.

Four Red-Crowned Crane carcasses were collected at four nesting sites: one adult Crane was collected in early April of 2010 at site S10 (body weight [BW]: 9.4 kg, male); two sub-adult Cranes were found in early November at site S13 (BW: 6.5 kg, female) and Site S15 (BW: 6.8 kg, male), and both dead Cranes had almost no residues in their stomach, but with few grass-seed and stems; and one adult Crane sample found in late October of 2012 at S17 (an obvious fracture injury was found in the right wing, BW: 8.3 kg, male). The direct death cause for these Crane samples was starvation because of food shortage in freezing condition according to a pathological inspection. The Cranes were immediately transferred to the laboratory for dissection. Approximately, 1 g to 2 g samples of livers, kidney and breast muscles were collected using a stainless steel knife. Polyethylene gloves were used throughout the all dissection procedures to prevent contamination. Some flight feathers were also collected from the Cranes and washed with distilled water in the laboratory.

All sediment samples were sieved through a 63 μm mesh after indoor air drying for acid digestion based on the method by Viklander (1998). After drying the reed rhizome, aquatic animal body, and feathers with filter papers, these samples were oven-dried to a constant weight (48 h at 60°C). The dried samples were ground to homogenous powders in a quartz bowl for acid digestion. Similar processes were performed on the liver, kidney and muscle samples, without washing and drying in the laboratory.

A total of 0.5 g of each sample was acid digested in a microwave and digested according to USEPA (1996) methods. Triplicate sub-samples of known dry weight were digested in an acid mixture (3 ml HNO3 + 1 ml HCl; Canli et al., 1998), and evaporated slowly to almost dryness (90°C). The residue was dissolved in 5 ml 1:1 diluted HCl, and then settled to 25 ml for analysis after the solution cooled down to room temperature.

The determination of As in the sediments, preys, muscles and organs together with flight feathers of the Cranes were performed by inductively coupled plasma-mass spectrometry (ICP-MS Agilent 7500ce, Agilent Technologies, Inc., USA). All of the materials used for sampling and analysis were acid-washed, and all of the samples were analyzed in triplicate with a relative standard deviation lower than 1.5%.

Geo-accumulation index (Igeo) was used to assess As accumulation in sediment as introduced by Muller (1969), expressed by the following empirical equation (Sekabira et al., 2010):
formula

where Cn is the measured concentration of a heavy metal in sediment and Bn represents the geochemical background value of metal n in unpolluted sediments. Igeo was classified as following:

Igeo< 0, background concentration; 0 < Igeo < 1, unpolluted; 1 < Igeo, polluted.

Results

The As concentration in the sediment were generally lower than that in the average natural background values (Figure 2a), except at site S5 and site S6, which varied from 0.34 ppm to 8.32 ppm. Almost all the As in the study area had exceeded the tolerable level (1 ppm to 1.7 ppm) for agro-economic crops suggested by Kabata-Pendias (2001), but below the tolerable level (10 ppm) for rice plants by Abedin et al. (2002).

The distribution characteristics of the As concentration, in general, correspond to the land use pattern and function zone of the wetland. High concentrations of As were found in the middle reaches and buffer zone of the wetland, wherein various agricultural and anthropogenic activities happen, e.g. industrial sludge and urban disposal. By contrast, low metal concentrations were identified in the core area, wherein anthropogenic sources were minimal. We grouped the samples into two classes by their ecological function zone (e.g. midstreams of Wuyur River and buffer zone versus core area). As concentration in the midstreams of Wuyur River and the buffer zone (average concentration of 3.38 ± 2.46 ppm) were significantly higher than those in the core area (average concentration of 1.21 ± 1.05 ppm) (F = 8.29, p = 0.01). The As contamination at all sampling sites was approximately equal to the background level (Igeo < 0) as assessed using the geo-accumulation index method (Table 1), suggesting background contamination in this region.

Reed rhizome and stem, as the preferred food of the Red-Crowned Cranes in Zhalong wetland, were found to contain measureable levels of As, with the following order of increasing concentration: stem < rhizome < root, as presented in Figure 2b. The results agree with the conclusion of Hughes et al. (1980) that heavy metals, such as As, although not readily soluble in sediments, are absorbed mainly by root hairs and are stored to a considerable degree in the roots. As concentrations in the reed rhizome and root varied from 0.45 ppb to 69.76 ppb and from 0.29 ppb to 27.14 ppb, respectively, the ranges of which were similar to the concentration range of carrot roots in U.S. (Kabata-Pendias, 2001). The bioaccumulation factor (BAF, defined as the ratio of detected metal concentration in reed root to its concentration in sediment) is widely used to investigate the role of plant in both cycling of trace metals and contaminating food chain (Malik et al., 2010). The BAF of As ranged from 0.00107 to 0.0178. The contents of these metals were linearly positively correlated with the concentrations in the sediment (r2 = 0.62, p < 0.01).

Pond Snails which are the primary consumers and whose preferred food is reed leaves and humus in sediments, accumulated relatively low As concentration. By contrast, the aquatic animals in the high trophic level of food chain (i.e. P. Dybowski and C. Sharp families which are the secondary consumers that prey mainly on fish and aquatic insect larvae) contained higher metal concentrations (Figures 3 and 4). The ratio of the As in the water animal was more than 5 times to 100 times that of the aquatic plant organ (i.e. reed stem), but was less than 10 times the ratio the second consumer (P. Dybowski)/primary consumer (Viviparidae), as shown in Table 1 and Figure 3.

The total As concentrations in the bodies of Pond Snails were much higher than in their shells as indicated by Figure 4a. The total As concentrations in the slug of Pond Snails (Viviparidae family) varied from 5.27 ppb to 22.84 ppb, with an average concentration of 11.48 ppb. Although As was observed in the C. Sharp and P. Dybowskistem, the concentrations of As in different sections also varied significantly (p < 0.001), i.e. As in the head section were larger than that in the intermediate and tail sections in the fish species, but As concentration in the remaining section was greater than that in the head section in the C. Sharp family (Figures 4b and c).

Concentrations in Cranes and other water birds (mainly Common Eider and Little Egret) are presented in Table 2. Endangered waterfowl (e.g. Red-Crowned Cranes) accumulated measureable levels of As, with an increasing order of feather < muscle < kidney < liver. High concentrations of the As were detected in the internal organs, such as liver and kidney. Feathers had the lowest metal contents, which varied from 23.12 ppb to 42.47 ppb. The kidneys and livers were the most prone to As accumulation, which is consistent with the conclusions of Takazawa et al. (2004) and Malik et al. (2010) that the liver and kidney of waterfowls are more prone to accumulate many toxic metals, such as As, than many other internal organs. Conversely, the muscle of the Red-Crowned Cranes in the Hokkaido, Northern Japan has larger As content than in the liver, with concentrations of 36 ppb and 29 ppb, respectively (fresh weight). The kidney of the Red-Crowned Cranes had the highest As concentrations, at 367.78 ppb.

Bioaccumulation can be one of the important threats for heavy metal exposure, apart from toxicity and persistence. The result agrees with the conclusion of Eilser (1988) that As is concentrated by organisms, but biomagnified in the food chain, i.e. the proportion of detected As concentration in the feather of Crane/the reed stem at site S10 was 6.73, but elevated to be 34.43 for feather/fish head at the same site. The ratio of As in the liver of the Red-Crowned Crane by the fish head (P. Dybowski) at site S10 demonstrated the largest bio-concentration. Similar to the As concentration variation, the bioaccumulation varied in different organs and tissue, with an increasing order of feather < muscle < kidney < liver, i.e. the BAFs of plume and liver of the Crane at S13 was 0.08/11.11/44.73 and 0.21/70.26/283, respectively. The evaluation result of the dietary exposure level of the migratory Red-Crowned Crane population in northeastern China is presented in Table 3. The daily intake of As of the Red-Crowned Cranes ranged from 2.39 ug day−1 to 2.68 ug day−1 per Crane.

Discussion

Agricultural practices (mainly the application of fertilizers and pesticides) contributed significantly to As contaminations in soils (Fleischer et al., 1974). The first set of sediment samples was located in the midstream of the Wuyur catchments, where runoffs flowing through from the large area of arable land would inevitably accumulate some As, that consequently enter the bird habitats, thereby elevating the concentration of As gradually (S1 < S2 < S3). Buffer zones A and B were adjacent to the arable area. Given that the areas are being cultivated, intensive anthropogenic activity induces high probability of crane contact with toxic chemicals, such as herbicides and insecticides. By contrast, the core area is protected by the buffer zone from local human impact to some extent, which may be the reason for the maximum total As was detected at S5 and S6, and for the minimal As in the core area. In addition, the most prevalent form of As in Zhalong wetland and most toxic to various water birds in the sediment was most likely to be inorganic form (i.e. arsenate and arsenate), according to previous research (Eisler, 1988; Kabata-Pendias, 2001), but further research is still recommended.

In this study, As contents in fishes varied in an increasing order of tail section < intermediate section < head section, consistent with the reports of Agah et al. (2009) and Malik et al. (2010) that gills of fish highly accumulate As. The presence of As in the aquatic animal did not indicate the contamination of particular sediments and habitants, because all of the measured As concentration in the water animals did not exceed the allowable concentration limit (1,000 ppb) recommended by Aghan et al. (2009). Although heavy metal accumulation in the migratory birds may also originate from wintering site, it can be concluded that the toxic risk by As imposed on the migratory Red-Crowned Crane population had low probability, because of the unpolluted state for As in both Zhalong wetland (breeding site for the migratory cranes) and Yancheng wetland (wintering site, Zuo et al., 2010). The highest As concentration value detected in the kidney of the Red-Crowned Crane at site S10, i.e. at 367.78 ppb, was significantly below the toxic level (10,000 ppb in fresh weight) as recommended by Eisler (1988). Although high concentrations of As is toxic, this element is an essential micronutrient for many species (Kabata-Pendias, 2001; Koller, 1980). Comparison of the conclusions of Burger et al. (2008) and Zhang et al. (2006), indicate that As concentration in the feather of the Red-Crowned Crane in Zhalong wetland were significantly lower than those in the Common Eider in Aleutian Island and Amchitak and Kiska areas and Little Egrets in Pearl Delta in southern China (p < 0.05). In addition, the daily intake (2.39 ug kg−1 to 2.68 ug kg−1) of the Red-Crowned Crane was significantly lower than the toxic level, i.e. at 120 mg kg−1 in the diet recommended by Eisler (1988). Hence, the dietary exposure level of the migratory Red-Crowned Crane population in China to As can be considered quite safe.

Conclusions

Generally, dietary exposure levels of As to the Red-Crowned Crane in China's Zhalong Wetland to total As were below toxicity threshold concentrations. Fairly low As concentrations in sediments contributed to a safe level of As content being accumulated in the prey of the Red-Crowned Crane: i.e. 0.29 ppb–69.76 ppb in reed and 5.27 ppb–22.84 ppb in the three aquatic animal species. A detectable level of As was observed in both internal and external tissues, in a range of 145.46 ppb to 367.78 ppb and 63.45 ppb to 257.46 ppb, respectively. The daily intake of As of these Cranes did not exceed a level considered to be potentially toxic in birds (i.e. 120 mg kg−1), ranging from 2.39 ug day−1 to 2.68 ug day−1 per crane.

Acknowledgements

We extend great appreciation to Professor Shane de Solla and another anonymous reviewer for their constructive advice for this manuscript.

Funding

This research was funded by the National Youth Science Foundation of China (Grant no. 41101034) and School of supporting youth's academic backbone project in Heilongjiang province of China (Grant no. 1253G063).

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