The environmental accumulation of trace elements is considered as a main threat for wildlife including various bird species (Beyer et al. 2000). Seabirds such as gull species have been used as a suitable bioindicator to evaluate the marine pollution, because these birds can be more sensitive to toxic elements than other vertebrates (Braune and Simon 2004) and because of their wide geographical distribution. In addition, they feed at the upper trophic levels of marine ecosystems and provide information on the extent of contamination in the whole food chain (Malinga et al. 2010; Savinov et al. 2003).

Chilsando Island, a breeding site of black-tailed gulls (Larus crassirostris) is far from anthropogenic sources of contamination found near urban, industrial and agricultural centers in temperate regions where emissions, effluents and runoff abound. As a permanent resident bird in Korea, black-tailed gulls can be exposed to various contaminants during their breeding season and migration after breeding including wintering ground. Geographical differences in trace element concentrations were found for black-tailed gulls in different breeding colonies in Korea (Kim and Oh 2014).

Adult and nestling birds differ in their age, body size and metabolism, which could affect the accumulation of trace elements (Nilsson and Råberg 2001). Toxic elements including Cd and Pb accumulate over time, resulting in increasing accumulation with age in birds (Kim and Oh 2016; Binkowski et al. 2013). The objectives of this investigation were to assess age-dependent accumulation of several trace elements (Cd, Pb, Cr, Al, Cu, Mn, Zn and Fe) in the liver of black-tailed gull adults and nestlings and examine the relationship among trace elements in the liver.

Materials and Methods

Black-tailed gulls (Larus crassirostris) are permanent residents and breed on uninhabitated islands in Korea. In 2011, there were approximately 14,000 pairs of black-tailed gulls at Chilsando Island, Jeollanam-do, Korea (Fig. 1).

Fig. 1
figure 1

Collecting site of black-tailed gull adults and nestlings in Korea, 2011

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Black-tailed gull nestlings (n = 10) and adults (n = 10) were collected at Chilsando Island (35°19′N latitude, E 126°16′E longitude), Jeollanam-do, Korea, in June 2011. The nestlings were marked with plastic rings 1–3 days after hatching and were recaptured 20–22 days after hatching from randomly selected nests (n = 10). Adults were caught in mist nets.

For adults and nestlings, body mass (0.1 g), culmen (0.1 mm) and tarsus (0.1 mm) length were measured. Adult and nestling gulls were euthanized by thoracic compression and frozen at −20 °C until necropsy. These birds were later thawed and the liver carefully removed from the samples, weighed (±0.1 g) and dried in an oven for 24 h at 105 °C until no further weight reduction occurred. Liver remainders were homogenized in a glass Teflon homogenizer and weighed (±0.1 g). All trace element concentrations (µg/g) in the liver were estimated on dry weight (dw) basis.

Approximately 2–3 g of each sample was digested in a mixture of concentrated nitric, perchloric and/or sulfuric acids in Kjeldahl flasks. Aluminum, Cu, Mn, Zn and Fe concentrations were determined by flame atomic absorption (AA) spectrophotometry (Hitachi Z-6100), after mineralization. Cadmium, Pb and Cr concentrations in the digested solutions were extracted with DDTC-MIBK (Kim and Oh 2015). Eight spikes and blanks were included in the analysis (about 20% of the total number of samples). A spike, a blank, a standard (0.01, 0.02, 0.03, 0.04, 0.05 ppm for Cd and Cr; 0.1, 0.2, 0.3, 0.4, 0.5 ppm for Pb and 1, 2, 3, 4, 5 ppm for Al, Cu, Mn and Zn) and a sample were run in triplicate in each analytical run. Spikes recoveries ranged from 94% to 106%. Recovered concentrations of the samples were within 5% of the certified values. Detection limits were 0.01 µg/g dry weight (dw) for Cr and Cd, 0.1 µg/g dw for Pb and 1.0 µg/g dw for Al, Cu, Mn and Zn (Kim and Oh 2015).

We statistically tested trace element concentrations for differences between adult and nestling black-tailed gulls using unpaired t tests. Data were log transformed to obtain a normal distribution that satisfied the homogeneity of variance assumptions of t-test (Kim and Oh 2014). Correlations of the concentrations between trace elements were examined using Pearson correlations (r). We present geometric means, 95% confidence intervals, arithmetic means and standard deviations in tables and texts. Statistical analyses were carried out using SPSS 13.0 version.

Results and Discussion

Adult gull livers had significantly greater concentrations of all elements than nestlings (Table 1); Cd (t test, p < 0.001), Pb, Cr, Al, Cu, Mn, Zn and Fe (t test, p < 0.01, respectively). Black-tailed gull adults had over ten times higher Cd concentration in the liver than that of the nestlings. Mean Pb concentration in the liver of the gull adults was over two times higher than that of the nestlings. The concentrations of Cr, Al, Cu, Mn, Zn and Fe in black-tailed gull adults were approximately 1.5 times greater than in the nestlings, respectively.

Table 1 Concentrations (geometric mean, 95% confidence intervals (CIs) and mean ± SD, µg/g dw) of trace elements in livers of black-tailed gull nestlings and adults
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In the liver black-tailed gull adults and nestlings, Cd and Cr concentrations were positively correlated with Al (r = 0.522, p < 0.01), Cu (r = 0.640, p < 0.01), Mn (r = 0.665, p < 0.01), Zn (r = 0.636, p < 0.01) and Fe (r = 0.692, p < 0.01), and Cd concentrations were positively correlated with Pb (r = 0.556, p < 0.05) and Cr (r = 0.616, p < 0.01); Pb concentrations were positively correlated with Fe (r = 0.686, p < 0.01) (Table 2).

Table 2 Correlation coefficient (r) between the concentrations of trace element in the liver of black-tailed gull adults and nestlings combined
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In the present study, toxic elements including Cd, Pb and Cr were greater in adults than in nestlings. The Cd accumulation (adults > nestlings) in the liver seen in this study has also been reported for other bird species. Liver concentrations of Cd in adult birds were higher than nestlings or juveniles on common kestrels (Falco tinnunculus) (Kim and Oh 2016), mallards (Anas platyrhynchos) (Binkowski et al. 2013), barrow’s goldeneyes (Bucephala islandica) (Ouellet et al. 2012), common grackle (Quiscalus quiscula) (Bryan et al. 2012), pied flycatchers (Ficedula hypoleuca) (Berglund et al. 2011), black-headed gulls (Larus ridibundus) (Orłowski et al. 2007; Migula et al. 2000), glaucous gulls (Larus hyperboreus) (Malinga et al. 2010; Riget et al. 2000) and little owls (Athene noctua) (Zaccaroni et al. 2003). However, there were no the accumulations of Cd in the liver of coots (Fulica atra) (Binkowski et al. 2013), great tits (Parus major) (Berglund et al. 2011) and black-tailed gulls (Agusa et al. 2005). In the liver, higher Pb concentrations in adults than in nestlings from this study and has been reported for other bird species. Concentrations of Pb were higher in adult than juvenile common kestrels and eurasian eagle owls (Bubo bubo) (Kim and Oh 2016), black-tailed gulls (Agusa et al. 2005) and little owls (Athene noctua) (Zaccaroni et al. 2003). In contrast, Pb concentrations in the liver did not differ between ages of mallards and coots (Binkowski et al. 2013), pied flycatchers and great tits (Berglund et al. 2011), marbled teals (Marmaronetta angustirostris) (Taggart et al. 2009) and black-headed gulls (Orłowski et al. 2007; Migula et al. 2000). In one study, barrow’s goldeneye juveniles had higher Pb concentrations than adults (Ouellet et al. 2012). Cr concentration in black-tailed gulls was elevated with age (this study; Agusa et al. 2005). In contrast, there were no differences in liver concentrations of Cr between ages of little owls (Athene noctua) (Zaccaroni et al. 2003).

In seabirds including gull species, Cd, Pb and Cr are generally associated with environmental contamination and diet (Kim and Oh 2014; Jerez et al. 2011; Malinga et al. 2010; Migula et al. 2000). These toxic elements in seabirds were influenced by their feeding ecology, intensity and time of exposure in foraging areas and the physiological and biochemical characteristics of these elements (Kim and Oh 2014; Jerez et al. 2011). These non-essential elements are known not to be metabolically regulated and markers of anthropogenic pollution (Metcheva et al. 2006).

In avian livers, Cd concentrations over 3 µg/g dw are suggestive of increased environmental exposure and are a tentative threshold effect levels (Scheuhammer 1987) associated with physiological and ecological problems including lethality (Beyer 2000). Black-tailed gull nestlings and adults (mean 0.05–0.53 µg/g dw) were well below this toxic threshold. In contrast, Cd concentrations in gulls at other locations were generally higher that reported in this study and some exceeded the 3 µg/g dw threshold. These studies included black-tailed gulls (mean 0.05–0.62 µg/g dw) (Kim and Oh 2014), glaucos gull chicks (0.28 2.51 µg/g dw) (Malinga et al. 2010), glaucos gulls and herring gulls (2.21–2.51 µg/g dw) (Savinov et al. 2003) and black-headed gull nestlings and fledglings (0.44–2.62 µg/g dw) (Migula et al. 2000) were within the background Cd levels in the liver. In contrast, glaucous gull adults (mean 5.46–6.40 µg/g dw) (Malinga et al. 2010), black-headed gulls (3.73, 16.8–28.6 µg/g dw) (Orłowski et al. 2007; Migula et al. 2000), black-tailed gull adults (4.80 µg/g dw) and juveniles (3.15 µg/g dw) (Agusa et al. 2005) and glaucous gulls (1.21–10.3 µg/g dw) and herring gull (Larus argentatus) nestlings and adults (4.28–48.0 µg/g dw) (Savinov et al. 2003).

In birds, background Pb concentrations in the liver were <6 µg/g dw and 10–20 µg/g dw can produce clinical signs of Pb poisoning in birds (Franson 1996). Black-tailed gull nestlings and adults (mean 0.24–4.09 µg/g dw) (this study; Kim and Oh 2014; Agusa et al. 2005) had the background Pb level. However, in black-headed gulls (8.86, 16.0–18.5 µg/g dw), Pb concentrations were elevated above the background level (Orłowski et al. 2007; Migula et al. 2000). Elevated Pb concentrations can have sublethal effects on birds including decreased body condition, reproductive success, behavior, immune response and physiology (Custer et al. 2009; Snoeijs et al. 2004; Migula et al. 2000).

Although the data are limited, geographical and taxonomic patterns of Cd and Pb concentrations in gulls tissues have been found in various gulls worldwide (Kim and Oh 2014; Malinga et al. 2010; Burger et al. 2009; Savinov et al. 2003; Migula et al. 2000) and Pb (Kim and Oh 2014; Burger and Gochfeld 2009; Burger et al. 2009; Migula et al. 2000). Concentrations of Cd were the highest in black-headed gull adults from Poland (Migula et al. 2000) and the lowest in black-tailed gull nestlings from Korea (this study). The highest Pb concentration was black-headed gull adults from Poland (Migula et al. 2000) and the lowest in black-tailed gull nestlings from Korea (this study). Also, Cd and Pb concentrations in black-tailed gulls from this study were relatively lower than other gull species worldwide. In general, concentrations of Cd and Pb may be attributed to differences in dietary exposure to contaminants at foraging sites and environmental quality (Savinov et al. 2003; Braune and Simon 2004; Schummer et al. 2011). In seabird chicks, elevated Pb concentrations were associated with historic Pb contamination in nearby buildings (Kim and Oh 2015; Finkelstein et al. 2003) and Pb-based fishing weights (Kim et al. 2013). At this study site, Pb contamination from buildings and fishing weights do not appear to be an issue.

Cr concentrations in the avian liver >4.0 µg/g dw are is associated with known to tentative toxicity (Eisler 2000) and with adverse effects such as embryo development, hatching success and viability of chicks (Custer et al. 2012; Kertész and Fáncsi 2003). In black-tailed gulls, Cr concentrations were much lower than the toxicity level (this study; Agusa et al. 2005).

In the present study, age-dependent accumulations (adults > nestlings) were found for Al, Cu, Mn, Zn and Fe. These trends have been reported for common kestrels for Cu and Fe (Kim and Oh 2016), glaucous gulls (Larus hyperboreus) for Cu, Mn, Zn and Fe (Malinga et al. 2010), marbled teal for Cu (Taggart et al. 2009) and black-tailed gulls for Cu, Mn and Zn, (Agusa et al. 2005).

The absorptions of essential elements including Al, Cu, Mn, Zn and Fe are regulated by homeostatic control, but elevated concentrations of these elements can cause adverse effects (Berglund et al. 2011; Custer et al. 2009, 2012). In the present study, Al, Cu, Mn, Zn and Fe concentrations in the liver of black-tailed gull adults and nestlings were within the background levels for birds. Concentrations of these elements except Al were comparable or lower than those of other gull species including black-tailed gulls and essential elements are probably maintained by a normal homeostatic mechanism (Kim and Oh 2014; Malinga et al. 2010; Agusa et al. 2005; Orłowski et al. 2007; Savinov et al. 2003). Al concentrations in this study were within the range of other normal concentrations from other bird species (Custer et al. 2012, 2009; Schummer et al. 2011).