Protected areas play an important role in the preservation of biodiversity through the protection of endangered species and ecosystems. They also serve as reservoirs of plant and animal species that can repopulate the devastated ecosystems. Hormod protected area, with a surface area of about 151,284 hectares is located in Larestan city, Fars Province, south of Iran (26°40′ to 27°N and 55°21′ to 55°52′E). Protected areas such as Hormod play an important role in protection of plant and animal species. The dense vegetation in the Hormod protected area, with a high diversity of plant species provides diverse habitats for birds like chukar, pigeon, lark and plover. In this paper, the concentrations of cadmium, lead, cobalt and copper in the kidney, liver and pectoral muscle of three species of wild birds in Hormod protected area, namely chukar (Alectoris chukar), see–see partridge (Ammoperdix griseogularis) and rock dove (Columba livia) are reported. These species are permanent resident birds in Iran. Although these bird species are protected by the Iranian Department of Environment, they are consumed by the local people.

Birds have been extensively used in the past as bioindicators of metal contamination in the environment (Burger 1994; Kim and Koo 2007; Mansouri et al. 2011). They are situated high on the food chain, can yield information over a large area around each sampling site, not only on bioavailability of contaminants but also on how, where, and when they are transferred within the food chain (Battaglia et al. 2005). Burger (1995) reported that birds can accumulate metals into their feathers, making feathers useful for biomonitoring of metals in the environment. Birds sequester metals in their feathers, where the proportion of the body burden is relatively constant for each metal (Barbieri et al. 2009). Although seabirds and shorebirds have been used in many studies, their characteristics of wandering and feeding over a large area make it difficult to determine where they have acquired the metals. Recently, some researchers explored the potential of monitoring metal pollution using wild species such as doves (e.g., Columba livia), pigeons (Forma urbana), and great tits (Parus major) (Janiga and Zemberyová 1998; Nam et al. 2004; Hoff Brait and Antoniosi Filho 2011). These species are ideal bioindicators because they are common and widely distributed and have fast metabolic rates. Hence, our study aimed to further investigate the concentrations of cadmium, lead, cobalt and copper in the feathers of chukar (A. chukar), see–see partridge (A. griseogularis) and rock dove (C. livia). The research was also to examine the species, gender and age-related variations in trace metal accumulation.

Materials and Methods

Bird samples were collected in February 2012 from the Hormod protected area. A total number of 45 bird samples of three bird species (15 of each species) were analyzed for cadmium, lead, cobalt and copper concentrations in their feathers. Breast feathers were selected because they are representatives of the plumage and are less influenced by the molt compared to flight feathers (Burger and Gochfeld 2000). The bird samples included chukar (A. chukar) (n = 15), see–see partridge (A. griseogularis) (n = 15), and rock dove (C. livia) (n = 15) with average weight (±SE) of 451 (±94), 268 (±91), and 367 (±115) g, respectively. The individuals were killed, weighed, stored in plastic bags, and kept at −20°C until dissection and chemical analysis. The feather samples were digested in a (2:1) nitric acid (HNO3) and perchloric acid (HClO4) solution (Merk, Germany). The feather tissues were then accurately weighed into 150-mL Erlenmeyer flasks, and 10 mL nitric acid (65 %) was added to each flask, and the samples were left overnight to be slowly digested (Mansouri et al. 2012); thereafter, 5 mL perchloric acid (70 %) was added to each sample. Digestion was continued on a hot plate (sand bath) at 200°C. After that, the digested samples were diluted by 25 mL deionized water. The concentrations of heavy metals were measured using a Shimadzu AA 680 flame atomic absorption spectrophotometer. The detection limits of metals were: cadmium (0.038 μg/g), lead (0.042 μg/g), cobalt (0.049 μg/g), and copper (0.038 μg/g). The mean recovery percentages of cadmium, lead, cobalt and copper were 98 %, 99 %, 103 %, and 97 %, respectively.

Statistical analyses were performed using the statistical package SPSS (version 16; SPSS, Chicago, IL). The concentrations of metals were compared in the feathers of chukar, see–see partridge, and rock dove species using two-way analysis of variance (ANOVA). We used a two-way ANOVA to study the metal concentrations and sex, age [sex × age] interactions. Data were log transformed to achieve normal distribution that satisfied the homogeneity of variance required by ANOVA. The concentrations of metals in feather tissues were expressed as microgram per gram dry weight (dw). Values are given in means ± standard errors (SE).

Results and Discussion

The mean concentrations of cadmium and lead in the feathers of A. chukar, A. griseogularis, and C. livia, collected from Hormod protected area in south of Iran are presented in Tables 1, 2, 3 and 4. The average cadmium concentrations were 2.0, 1.9, and 1.9 μg/g for A. chukar, A. griseogularis, and C. livia, respectively. The average lead concentrations were 8.0, 5.4, and 7.7 μg/g for A. chukar, A. griseogularis, and C. livia, respectively. No significant difference was observed between the average concentrations of cadmium and lead in the feathers of these three species (one-way ANOVA, p > 0.05). Among these three species, the highest cadmium concentration was found in the feathers of female/adult birds and the lowest cadmium concentration was observed in the feathers of female/juvenile birds. The highest lead concentration was measured in female/adult birds and the lowest lead concentration was found in male/juvenile birds (except A. chukar). Overall, the concentrations of cadmium and lead in adult birds were higher than in juveniles. The concentrations of cadmium were higher in females than in males.

Table 1 Mean (±SE) metal concentrations (μg/g dry weight) in the feathers of Alectoris chukar in Hermoud protected area in southern Iran
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Table 2 Mean (±SE) metal concentrations (μg/g dry weight) in the feathers of Ammoperdix griseogularis in Hermoud protected area in southern Iran
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Table 3 Mean (±SE) metal concentrations (μg/g dry weight) in the feathers of Columba livia in Hermoud protected area in southern Iran
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Table 4 The analysis of variance (ANOVA) of the data among species
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Cadmium and lead are very toxic and common in the environment. Elevated cadmium concentrations in the feathers were strongly correlated with reduced growth rates of bone (Spahn and Sherry 1999) but not mass (Custer and Mulhern 1983) in wild birds. Cadmium and lead concentrations in the feathers of these three bird species were higher than those in great tits and robins in central Portugal (Costa et al. 2011), and little owls and common buzzards in northern Italy (Battaglia et al. 2005). Several studies have suggested that lead in feathers can be partially due to direct external contamination onto the feather surface (Burger 1993; Dauwe et al. 2002a). Goede and de Voogt (1985) reported lead concentrations of 1.0–32.0 μg/g dry weight in feathers of the Wadden Sea’s shorebirds. Lead concentrations of 4 μg/g dry weight in feathers are known to cause sublethal and reproductive effects (Kim and Koo 2008). In this study, lead concentrations were greater than 5 μg/g in the feathers of the three species. The high concentrations of lead in the feathers indicate that the environment is highly polluted with lead. As with other studies, this research suggests that feathers could be used to indicate local atmospheric contamination (Almansour 2007; Dauwe et al. 2002a). Lead as an ubiquitous pollutant is transported into the sea by industrial wastewater, produced by industries such as printing, dyeing, and oil refineries (Lakshmanan et al. 2009; Newbury 1979).

Essential elements, such as copper (Cu) and cobalt (Co) are necessary for the metabolism but can cause adverse effects when their concentrations in the organism become excessive. Cobalt as part of vitamin B12 is associated with nitrogen assimilation, and synthesis of hemoglobin and muscle protein. In addition, cobalt influences certain enzymes (Roginski and Mertz, 1977). However, excessive intake of cobalt by organisms results in toxic effects. The highest cobalt concentrations in these three species were measured in female/adult birds and the lowest concentrations were found in female/juvenile birds. Idem, in the three species, the highest copper concentrations were measured in female/adults and the lowest concentrations were observed in male/juveniles (except C. livia). The average concentrations of cobalt and copper were 1.2 and 9.8 μg/g, 1.5 and 9.7 μg/g, and 1.3 and 10.4 μg/g dry weight in A. chukar, A. griseogularis, and C. livia, respectively. Copper concentrations found in this study were similar to those in great tits (Llacuna et al. 1995) and great and blue tits in Antwerp, Belgium (Dauwe et al. 2002b). In general, birds retain a small portion of copper and other metals ingested (Bryan and Langston 1992). Breteler (1984) reported that copper is one of the major threats to ecosystem health relative to other heavy metals. According to Schmitt-Jansen et al. (2008), the sublethal effects of copper on birds include growth retardation, suppression of egg production, thinner egg shells, and changes in behavior.

Several studies have examined the effects of gender and age on the accumulation of metals in feathers and other tissues (Burger 1995; Zamani-Ahmadmahmoodi et al. 2009; Mansouri et al. 2011). Few studies reported no significant differences in metal content of feathers between male and female birds (Hutton 1981; Zamani-Ahmadmahmoodi et al. 2009). Similarly, in this study no significant differences found between the concentrations of metals in male and female birds except lead in A. chukar (two-way ANOVA, p > 0.05), suggesting that different sexes utilize similar foraging strategies in these species (Hindell et al. 1999). However, females can sequester metals in eggs (Tom et al. 1999) which provides them with a unique route of elimination, not available to males (Burger 1993). On the other hand, significant differences were observed between the concentrations of lead and cobalt in A. chukar; cadmium, lead and copper in A. griseogularis; and cobalt and copper in C. livia; in adult and juvenile birds. Mansouri et al. (2011) found that the concentrations of cadmium and lead were higher in the feathers of adults than in juveniles of Egretta gularis and Larus heuglini. According to Furness and Monaghan (1987), cadmium concentration is always higher in the adults, because of bioaccumulation. Adults have had several years to bioaccumulate metals in their internal tissues, and this can be mobilized into the blood and deposited in feathers during their formation (Burger 1994).