Ecotoxicology (2009) 18:61–68 DOI 10.1007/s10646-008-0257-2
Heavy metal concentrations in three shorebird species from Okgu Mudflat, Gunsan, Korea Jungsoo Kim Æ Hwa-Su Lee Æ Tae-Hoe Koo
Accepted: 11 August 2008 / Published online: 2 September 2008 Ó Springer Science+Business Media, LLC 2008
Abstract Iron, zinc, copper, lead, and cadmium were measured in livers of three shorebird species from Okgu Mudflat, Korea in the East Asian-Australian migration flyways. Iron concentrations in red-necked stints (Calidris ruficollis) (geomean = 1,322 lg/g dw) were higher than in terek sandpipers (Xenus cinereus) (467 lg/g dw), and great knots (Calidris tenuirostris) (158 lg/g dw). Copper concentrations in great knots (85.8 lg/g dw) were significantly higher than in red-necked stints (15.9 lg/g dw) and terek sandpipers (10.4 lg/g dw). However, significant differences in zinc concentrations were not found in livers among shorebird species. Iron, zinc, and copper concentrations from this study were within the range of other shorebird studies. We suggest that essential elements such as iron, zinc, and copper are within normal range and are maintained there by normal homeostatic mechanism. Lead and cadmium concentrations differed among shorebird species; red-necked stints (geomeans 27.8 lg/g dw and 4.69 lg/g dw, respectively) were higher than in terek sandpipers (12.9 and 0.44 lg/g dw, respectively), and great knots (5.43 and 0.29 lg/g dw, respectively). Some rednecked stints exceeded toxic levels of lead and cadmium for wild birds. In livers of red-necked stints from Okgu Mudflat,
J. Kim H.-S. Lee T.-H. Koo (&) Department of Environmental Science and Engineering, Kyung Hee University, Yongin, Gyeonggi-do 446-701, Republic of Korea e-mail:
[email protected] J. Kim e-mail:
[email protected] H.-S. Lee e-mail:
[email protected]
lead and cadmium concentrations were higher than previously reported in other shorebirds. Keywords Shorebirds Livers Essential elements Lead and cadmium Poisoning level
Introduction The Okgu Mudflat, Gunsan City, Korea is recognized for its large populations of migrating and wintering shorebirds; more than 100,000 shorebirds are counted at the height of spring and autumn migration (Yi 2001). Shorebirds forage in the large expanse of mud flats and roost in the adjacent salt farm in the surrounding Okgu Mudflat. Okgu Mudflat is one of the major stopover sites for shorebirds in the East Asian-Australian migration flyways. Waders of the East Asian-Australian migration flyways are well known in the world, and many studies on migration routes and banding have been conducted in the Korean Peninsula (Yi et al. 1994). However, little research on pollutants has been conducted (Kim et al. 2007; Kim and Koo 2008). Shorebird species are territorial and defend small foraging areas during the winter (Myers et al. 1979). In radiotracking studies, some shorebirds showed a high degree of site fidelity to preferred habitat areas a few square kilometers in size (Warnock and Takekawa 1996) and moved a mean distance of\2.5 km between roost and foraging sites (Warnock and Takekawa 1995). These authors suggested that shorebirds foraging in polluted areas of their habitat may be exposed to much higher levels of contaminants than would be expected if they ranged freely among several different foraging areas in the estuary. Similarly, Ohlendorf et al. (1986) detected site-specific variation in contaminants in surf scoters (Melanitta perspicillata). Variation in
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contaminant levels at different sites might be reflected in the body burdens of shorebirds collected at the breeding or wintering ground. Also, different shorebird species at the same wintering sites and stopover sites may have different metal burdens because of the utilization of slightly different niches (Burger et al. 1993; Kim et al. 2007). Several physiological and biological processes, such as feeding habits, growth, age, reproductive stage, molting, and migration, may influence metal concentration and distribution in birds (Cheney et al. 1981; Honda et al. 1986). Lead and cadmium are widespread pollutants, distributed throughout all ecosystems. Lead is one of the main causes of poisoning through direct or indirect exposure from sinkers and lead shot (Johansen et al. 2004) and from lead-based gasoline (Burger et al. 1992). In addition, Bull et al. (1983) reported the death of shorebirds from consuming prey contaminated with lead. Cadmium poisoning has been widely recognized as triggering serious diseases. Cadmium disposal into the environment is severely restricted in many countries (Asami 2001; Friberg et al. 1974). The objectives of this study were to determine levels of iron, zinc, copper, lead, and cadmium in three shorebird species from Okgu Mudflat, Gunsan City, Korea in the East Asian-Australian migration flyway and to examine the correlation among these heavy metals. We hypothesized that Korean shorebirds have different heavy metal burdens due to the differences in heavy metal exposure at their breeding or wintering ground.
Materials and methods Twenty-nine individuals of three shorebird species were collected on Okgu Mudflat (35°530 N, 126°410 E), Gunsan City, Korea during spring and autumn migration in 1999– 2000 (Fig. 1). The collections included red-necked stints (C. ruficollis) (n = 12), terek sandpipers (X. cinereus) (n = 9), and great knots (C. tenuirostris) (n = 8). We collected red-necked stints and terek sandpipers in May, 1999 and 2000; great knots were collected in October, 2000. All birds were captured by mist netting with legal permission. The specimens were killed, weighed, stored in plastic bags, and kept at -20°C until dissection and analysis. Livers were dissected from the bodies of the specimens and analyzed for metals. We obtained sediment data (n = 91) from Kim et al. (2003). Iron, zinc, and copper concentrations were determined by flame atomic adsorption (AA) spectrophotometry (Hitachi Z-6100), after mineralization of samples with nitric, sulfuric, and perchloric acid in Kjeldahl flasks. Livers with low lead and cadmium concentrations were measured by AA spectrophotometry, after treatment with sodium N,Ndiethyldithiocarbamate trihydrate ((C2H5)2NCS2Na3H2O)-
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J. Kim et al.
Fig. 1 Collection location for shorebirds in 1999–2000, from Okgu Mudflat, Gunsan City, Jeollabuk-do, Korea
methyl isobutyl ketone (CH3COCH2CH(CH3)2) (DDTCMIBK) (Kim et al. 2008). Spikes and blanks were run at least seven times (more than 20% of the total number of samples). To assess accuracy, a spike, a blank, a standard, and a sample were run in triplicate in each analytical run. Spike recoveries ranged from 95% to 106%. Recovered concentrations of the certificated values were within 5% of the certificated values. All element concentrations in livers were estimated on a dry-weight basis (lg/g dw). In references, wet-weight concentrations (lg/g ww) were multiplied by a factor of 3 to estimate dry-weight concentrations (Clark and Scheuhammer 2003). Detection limits were 1.0 lg/g for iron and zinc, 0.1 lg/g for copper and lead, and 0.01 lg/g for cadmium. Concentrations of heavy metals were compared among livers of the three shorebird species using one-way analysis of variance (ANOVA). To compare all heavy metal residues, Bonferroni tests were used. The Bonferroni tests were used to separate species means following a significant ANOVA. Data were log transformed to obtain normal distributions that satisfied the homogeneity of variance required by ANOVA (Custer et al. 2003). Correlations among heavy metal concentrations were assessed using
Heavy metal concentrations in three shorebird species
63
Table 1 Heavy metal concentrations (geomean, 95% CI lg/g dw) in livers of shorebirds from Okgu Mudflat, Korea in 1999–2000 Species Terek sandpiper (n = 9)
Great knot (n = 8)
Red-necked stint (n = 12)
Iron
Zinc
Copper
Lead
Cadmium
Geomean
467a1
82.5
10.4b
12.9b
0.44b
Mean ± SD
604 ± 377
93.8 ± 36.0
11.6 ± 5.56
15.9 ± 11.9
0.82 ± 1.12
Extremes
82.8–1,181
15.9–133
4.15–22.3
6.38–42.7
0.04–3.73
Geomean
158b
85.8
21.7a
5.43c
0.29b
Mean ± SD
166 ± 55.3
140 ± 151
25.7 ± 18.5
5.76 ± 2.14
0.45 ± 0.53
Extremes
186–242
15.4–469
12.1–67.7
3.05–54.3
0.11–1.70
Geomean
1322a
33.6
15.9b
27.8a
4.69a
Mean ± SD
3,007 ± 4,171
91.8 ± 148
16.6 ± 5.73
29.4 ± 10.6
17.5 ± 22.1
Extremes
110–14,033
1.84–475
10.5–30.1
16.9–9.68
0.11–64.8
0.024
NS
0.043
\0.001
0.001
p-value NS = not significant 1
Means sharing the same letter were not significantly different among species
Pearson correlations (r). Statistical analyses were carried out using SPSS version 12.0. We present geometric and arithmetic means, and standard deviation in tables and text.
Among all combination of the five heavy metals, only lead and cadmium concentrations in livers of the three shorebird species were significantly correlated (r = 0.607, p \ 0.01) (Table 2).
Results Discussion Iron concentrations in livers of red-necked stints and great knots were higher than those in livers of terek sandpipers (ANOVA, p = 0.024). Zinc concentrations did not differ among shorebird species. Copper concentrations were higher in great knots than in red-necked stints and in terek sandpipers (ANOVA, p = 0.043). Lead concentrations in livers were higher in red-necked stints than in terek sandpipers, which in turn were higher than in great knots (ANOVA, p \ 0.001). Cadmium concentrations in rednecked stints were higher than in terek sandpipers and in great knots (ANOVA, p = 0.001) (Table 1).
Table 2 Correlation coefficient (r) between the concentrations of iron, zinc, copper, lead, and cadmium in livers of shorebirds from Okgu Mudflat, Korea in 1999–2000 Metal pair
r
No. of data pairs (N)
p-value
Lead–cadmium Lead–copper
0.607 -0.105
28 28
\0.01 NSa
Lead–zinc
-0.005
27
NS
Lead–iron
0.325
27
NS
Cadmium–copper
0.068
28
NS
Cadmium–zinc
0.260
27
NS
Cadmium–iron
0.338
27
NS
Copper–zinc
0.009
27
NS
Copper–iron
-0.051
27
NS
Zinc–iron
-0.064
27
NS
a
NS = not significant (p [ 0.05)
Heavy metal concentrations The essential elements iron, zinc, and copper measured in livers of shorebirds in this study were within the ranges normally found in other shorebirds (Blomqvist et al. 1987; Lee et al. 1987; Hui 1998; Hui et al. 2001; Kim et al. 2007) and are probably maintained there by normal homeostatic mechanisms for shorebird species. Iron concentrations in livers of the three Korean shorebirds were significantly different. In contrast, in southern California, Hui (1998) reported no differences between black-billed plovers (Pluvialis squatarola) and willets (Catoptrophorus semipalmatus) but reported differences between male and female in black-billed plovers but not in willets. In the Baltic Sea, iron concentrations in livers of dunlins (Calidris alpina) (geomean = 463 lg/g ww) and curlew sandpipers (Calidris ferruginea) (550 lg/g ww) were similar (Blomqvist et al. 1987). Zinc concentrations in Korean shorebird species from this study were well below the level associated with zinc toxicosis and poisoning. In wild birds, Gasaway and Buss (1972) suggested 1,200 lg/g dw in livers as a threshold level for zinc toxicosis, Levengood et al. (1999) found clinical signs of zinc poisoning in mallards with liver concentrations of 473–1,990 lg/g dw (Levengood et al. 1999), and Sileo et al. (2003) diagnosed zinc poisoning in wild waterfowl with liver concentrations of 280–2,900 lg/ g dw. In addition, Takekawa et al. (2002) found a negative
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64 Table 3 Copper concentration (arithmetic mean lg/g dw) in livers of shorebirds from various locations worldwide
J. Kim et al.
Species
Site
Level Source; collected year
Yeongjong Is.
16.5a Kim et al. (2007); 1994–1995
Korea Kentish plover Terek sandpiper Great knot
Okgu
11.6
Yeongjong Is.
19.1a Kim et al. (2007)
This study; 1999–2000
Okgu
25.7
This study a
Yeongjong Is.
10.6
Red-necked stint
Okgu
16.6
Mongolian plover
Yeongjong Is.
16.0a Kim et al. (2007)
Dunlin
Yeongjong Is.
25.9a Kim et al. (2007)
Ottenby, Sweden
13.7a Blomqvist et al. (1987); 1981–1983
Kim et al. (2007) This study
Europe Dunlin
16.9a
Curlew sandpiper Common snipe
Albufera de Valencia, Spain
19.0
Mateo and Guitart (2003); 1986–1995
North America a
Original data were on wet basis, but were converted to dry basis (93)
b
High value in males and females
c
High value from Hayward and Newark sites in San Francisco Bay
Willets Southern California Black-bellied plovers
24.9b Hui (1998); 1994 18.3b
Long-billed dowitcher
24.3c Hui et al. (2001); 1991–1992
South San Francisco Bay, California
Western sandpiper
24.7
South America Sanderling
Chile
Whimbrel
relationship between zinc concentrations and body mass. Zinc is known to interact with many chemicals to produce altered patterns of accumulation, toxicity, and metabolism (Eisler 2000). In general, birds with higher cadmium concentrations also have high zinc in tissues (Kim et al. 1996; Kim et al. 2008). In other Korean studies, zinc concentrations in livers were higher from Yeongjong Island (Kim et al. 2007) than from this study for great knots, but in livers of terek sandpipers the pattern was the opposite. Copper concentrations in birds are often elevated in areas of human activity and intensive copper use (Eisler 2000). Variation of copper concentrations is not attributed to contamination or higher natural background of copper in habitat of birds but to species-specific bioaccumulation factors mediated by metabolism (Honda et al. 1986; Kim et al. 1996). Copper concentrations in livers of shorebirds were higher at locations in Chile that were contaminated with tailings from copper mines. In this and other Korean studies, copper concentrations in livers of shorebirds range from 10.6 to 25.9 lg/g dw and were highest in dunlins from Yeongjong Island (Table 3). However, there is no data on the threshold effects levels of copper in livers for wild birds. In waterfowl, elevated copper concentrations (478–2,571 lg/g dw) were reported (Parslow et al. 1982; Mateo and Guitart 2003; Taggart et al. 2006). Additionally, after a mine spill in Don˜ana Natural Park, Spain, the mean copper concentrations found in birds that died in the natural
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30.6a Vermeer and Castilla (1991); 1981– 1982 27.2a
park were higher than those found outside the national park (Mateo and Guitart 2003). All great knots in this study had background levels of lead, but four red-necked stints and one terek sandpiper exceeded the toxic level for wild birds ([approximately 30 lg/g dw) (Clark and Scheuhammer 2003). The mean lead concentrations in red-necked stints were much higher than in shorebirds from other studies (Table 4). Bull et al. (1983) reported that lead has been responsible for acute incidents of shorebird poisoning: dunlins found sick had mean liver lead concentrations of 9 lg/g dw. Marbled godwits (Limosa fedoa) found dead after ingesting lead shot had liver lead concentrations of 52 lg/g ww (Locke et al. 2001). In this and other Korean studies, lead concentrations in livers of terek sandpipers from Okgu Mudflat were much higher than those from Yeongjong Island (Kim et al. 2007) and Nakdong River (Lee et al. 1987). Liver concentrations of lead in great knots were less in Okgu Mudflat than in Yeongjong Island (Kim et al. 2007). Lead concentrations in tissues of wild birds vary in relation to dietary concentrations (Ferns and Anderson 1997; Kim and Koo 2008). In our study, average concentrations of cadmium were at background concentrations in livers of terek sandpipers and great knots. However, cadmium concentrations in rednecked stints exceeded background levels with only two red-necked stints having background concentrations. Ferns and Anderson (1994) described a correlation between
Heavy metal concentrations in three shorebird species Table 4 Average lead concentration (arithmetic mean lg/g dw) in livers of shorebird from various locations worldwide
Species
65
Site
Level
Source; collected year
Kentish plover
Yeongjong Is.
14.3a
Kim et al. (2007); 1994–1995
Terek sandpiper
Okgu
15.9
This study; 1999–2000
Yeongjong Is.
3.60a
Kim et al. (2007)
Nakdong River
0.12a
Lee et al. (1987); 1979–1986
Korea
Great knot
Okgu
5.76
This study
Yeongjong Is.
12.8a
Kim et al. (2007)
Red-necked stint
Okgu
29.4
This study
Mongolian plover
Yeongjong Is.
6.15a
Kim et al. (2007)
Dunlin
Yeongjong Is.
11.3a
Kim et al. (2007)
Nakdong River
ND
Lee et al. (1987)
Lindisfarne, UK
10.5
Evans and Moon (1981); unknown
Europe Curlew Bar-tailed godwit
2.70
Dunlin Curlew sandpiper
Ottenby, Sweden
0.12a 0.18a
Blomqvist et al. (1987); 1981–1983
Dunlin
Bristol Channel, UK
4.20
Ferns and Anderson (1997); 1979–1980
Common snipe
Albufera de Valencia, Spain
1.70
Mateo and Guitart (2003); 1986–1995
0.81
White et al. (1980); 1976–1977
North America Dunlin
Texas coast, USA
Least sandpiper
0.60
Sanderling
3.09
Western sandpiper Willets
2.49 Southern California
Black-bellied plovers ND: not detected
Long-billed dowitcher
a
Original data were on wet basis, but were converted to dry basis (93)
ND
Hui (1998); 1994
ND South San Francisco Bay, California
Western sandpiper
cadmium concentrations in invertebrates and birds and concentrations found in sediments. The routes of transmission of cadmium from water and sediments to invertebrates are complex (Bryan and Langston 1992). In this and other Korean studies, cadmium concentrations in livers of terek sandpipers from Nakdong River (Lee et al. 1987) were much higher than those from Yeongjong Island (Kim et al. 2007) and Okgu Mudflat. Cadmium concentrations in great knots were higher at Yeongjong Island (Kim et al. 2007) than at Okgu Mudflat. The mean cadmium concentrations in red-necked stints from Okgu Mudflat (geomean = 4.69 lg/g dw, arithmetic mean = 17.5 lg/ g dw) and from Chile (approximately 16.2 lg/g dw, Vermeer and Castilla 1991) were due to contamination from tailings of a copper mine and were much higher than in other shorebird studies. Cadmium concentrations in shorebirds exceeded background levels (\3 lg/g dw) for wild birds in terek sandpiper from Nakdong River, red-necked stints from Okgu Mudflat, Korea, in oystercatchers (Haematopus ostralegus) from Wadden Sea, in black-bellied plovers from
ND
Hui et al. (2001); 1991–1992
ND
Southern California, and sanderlings (Calidris alba) and whimbrels (Numenius hudsonicus) from Chile (Table 5). Differences of heavy metal concentrations between shorebird species In this study, heavy metal concentrations in livers of shorebirds were different among shorebird species. Differences among shorebirds have also been reported for shorebirds using the same habitat (Davis and Smith 1998; Kim et al. 2007), between wild bird species from other studies (Custer et al. 2003; Kim and Koo 2007, 2008); and in feathers of different between shorebird species (Burger et al. 1993; Kim and Koo 2008). No differences were reported in metal concentrations between western sandpipers (Calidris mauri) and long-billed dowitchers (Limnodromus scolopaceus) (Hui et al. 2001); Hui (1998) reported differences between sexes, collection periods, and habitats of some heavy metal concentrations in livers of black-bellied plovers and willets.
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66 Table 5 Average cadmium concentration (arithmetic mean lg/g dw) in livers of shorebird from various locations worldwide
J. Kim et al.
Species
Site
Level
Source; collected year
Kentish plover
Yeongjong Is.
1.65a
Kim et al. (2007); 1994–1995
Terek sandpiper
Okgu
0.82
This study; 1999–2000
Yeongjong Is.
1.35a
Kim et al. (2007)
Nakdong River
3.93a
Lee et al. (1987); 1979–1986
Korea
Great knot
Okgu
0.45
This study
Yeongjong Is.
1.98a
Kim et al. (2007)
Red-necked stint
Okgu
17.5
This study
Mongolian plover
Yeongjong Is.
0.51a
Kim et al. (2007)
Dunlin
Yeongjong Is.
2.10a
Kim et al. (2007)
Nakdong River
2.22
Lee et al. (1987)
Ottenby, Sweden
0.78a
Blomqvist et al. (1987); 1981–1983
Europe Dunlin
2.28a
Curlew sandpiper Oystercatcher Common snipe
Wadden Sea Albufera de Valencia, Spain
7.58b 1.00
Stock et al. (1989); 1986–1987 Mateo and Guitart (2003); 1986–1995
Southern California
2.87b
Hui (1998); 1994
North America Willets
7.90b
Black-bellied plovers Original data were on wet basis, but were converted to dry basis (93)
Long-billed dowitcher
b
South America
a
High value in male or female
c
High value from Hayward and Newark sites in San Francisco Bay
South San Francisco Bay, California
Chile
Whimbrel
Interspecific differences in metal concentrations can arise even if the species share the same stopover and wintering grounds because shorebirds forage at different parts of the beach depending on tidal cycles (Connors et al. 1981) and different depths (Barbosa and Moreno 1999) based on their bill length (Paulson 1993). When shorebirds congregate into large, mixed-species aggregations, they may partition themselves into different microhabitats (Recher 1966; Yi 2001). Shorebirds feeding in the same stopover or wintering ground, may segregate into different microhabitats which have different contaminant concentrations. Moreover, shorebird species can have different metal burdens at stopover sites despite having the same wintering site (Burger et al. 1993; Davis and Smith 1998). These authors suggest that shorebirds consumed a varied diet even within the same feeding habits and this results in differences in heavy metals concentrations among shorebird species. Relation between heavy metal concentrations in livers and the environment Lead concentrations in sediment were higher in Bristol Channel, UK than in Okgu Mudflat and Yeongjong Island, but lead concentrations in livers of dunlins were much
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Hui et al. (2001); 1991–1992
1.23c
Western sandpiper Sanderling
1.15c
16.2a
Vermeer and Castilla (1991); 1981–1982
131a
higher at Yeongjong Island than at Bristol Channel, UK; concentrations in great knots were higher from Yeongjong Island than from Okgu Mudflat (Table 6). Cadmium concentrations in shorebirds were elevated in mudflats with high cadmium concentrations (Table 6). Our results suggest no lead bioaccumulation from sediment to livers of great knots. A lack of bioaccumulation of lead from sediment to birds was also reported in herons and egrets from Pakistan (Boncompagni et al. 2003) and in shorebirds from Bristol Channel, UK (Ferns and Anderson 1997). In Korea, shorebird species stayed for only a limited time (2–3 weeks) in Okgu Mudflat and Yeongjong Island; these areas were used merely as short-term stopover sites (Yi 2001). Therefore, we suggest that lead and cadmium concentrations in sediment was not incorporated to any degree into the tissues of shorebirds in Korea, and that lead and cadmium concentrations in shorebirds were more reflective of their breeding and wintering ground concentrations than of stopover site contamination. In conclusion, iron, zinc, lead, and cadmium concentrations were different among shorebird species. In particular, lead and cadmium concentrations were much higher in red-necked stints than in terek sandpipers and in
Heavy metal concentrations in three shorebird species Table 6 Lead and cadmium concentrations (arithmetic mean lg/g dw) in sediments and in shorebird livers from Okgu Mudflat and Yeongjong Island, Korea and Bristol Channel, UK
67
Sediment
Species
Source
Dunlin
Great knot
11.3
12.8
Lead Okgu
26.1
Yeongjong Is.
14.3
Bristol Channel
58.6–97.4a
5.76 4.2
Kim et al. (2003); this study Park (2002), Kim et al. (2007) Ferns and Anderson (1994)
Cadmium a
Mean range by site in Bristol Channel
Okgu
ND
0.45
Kim et al. (2003); this study
Yeongjong Is.
0.90 ± 2.86
1.98
Park (2002), Kim et al. (2007)
great knots from Okgu Mudflat, Korea. Concentrations in some red-necked stints exceeded a toxicity threshold for lead and cadmium for wild birds. However, lead and cadmium concentrations in shorebirds were not consistent with sediment concentrations at the migration stopover site (Okgu Mudflat) where shorebirds stayed only about 2–3 weeks. Therefore, we suggest that lead and cadmium concentrations in shorebirds from this study were more reflective of their breeding and wintering ground concentrations than of these stopover sites. Additional, detailed investigations will be necessary to analyze the prey materials and sediment of shorebirds and their habitat. Acknowledgment We are grateful to Thomas W. Custer (USGS) for critical reading of the manuscript and Christine M. Custer (USGS) for editorial assistance.
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