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Application of Brown Bear (Ursus arctos) Records for Retrospective Assessment of Mercury a
b
Eisa Solgi & Seyed Mahmoud Ghasempouri a
Department of Environment, Faculty of Natural Resources and Environment, Malayer University, Hamedan, Iran b
Department of Environment, Faculty of Natural Resources and Marine Science, Tarbiat Modares University, Noor, Mazandaran, Iran Published online: 03 Mar 2015.
Click for updates To cite this article: Eisa Solgi & Seyed Mahmoud Ghasempouri (2015) Application of Brown Bear (Ursus arctos) Records for Retrospective Assessment of Mercury, Journal of Toxicology and Environmental Health, Part A: Current Issues, 78:5, 342-351, DOI: 10.1080/15287394.2014.968816 To link to this article: http://dx.doi.org/10.1080/15287394.2014.968816
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Journal of Toxicology and Environmental Health, Part A, 78:342–351, 2015 Copyright © Taylor & Francis Group, LLC ISSN: 1528-7394 print / 1087-2620 online DOI: 10.1080/15287394.2014.968816
APPLICATION OF BROWN BEAR (Ursus arctos) RECORDS FOR RETROSPECTIVE ASSESSMENT OF MERCURY Eisa Solgi1, Seyed Mahmoud Ghasempouri2 1
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Department of Environment, Faculty of Natural Resources and Environment, Malayer University, Hamedan, Iran 2 Department of Environment, Faculty of Natural Resources and Marine Science, Tarbiat Modares University, Noor, Mazandaran, Iran Because mercury (Hg) is released into the atmosphere, wildlife living in habitats located far from point sources of metal may still be at risk. Mercury accumulation, previously considered a risk for aquatic ecosystems, is also found in many wildlife terrestrial species. The aim of the present study was to examine total Hg concentrations in the brown bear (Ursus arctos) by measurement of metal in hair from museum collections in Iran. Another objective of this investigation was to characterize the risk of Hg exposure in bears in several parts of Iran. Brown bear (Ursus arctos) hair samples (n = 35) were collected from 14 provinces in Iran for analysis of Hg contamination, performed using an advanced mercury analyzer (model Leco 254 AMA, USA) according to ASTM standard D-6722. Total Hg levels in Iranian bears from all areas ranged from 115.81 to 505.82 µg/kg, with a mean of 193.39 ng/g. Mercury concentrations in brown bear hair from different provinces in Iran were as follows in descending order: Khorasan Razavi > Esfahan > Khozestan > Yazd > Lorestan > Charmahalva Bakhtiari > Bushehr > Mazandaran > Markazi > Tehran > Ardebil > Gilan > East Azerbaijan. The highest content of Hg was found in the south (206.62 ± 31.95 ng/g), whereas the lowest levels were detected in the west (167.71 ± 32.97 ng/g). Overall total Hg content in bear hair was below harmful levels for this species. A decreasing trend was noted in the period 1986–2006, which may be mainly due to reduction of global Hg emissions. Data suggest that food habits and habitat are two important factors that influence Hg accumulation in bears.
wastes, cement plants, and chemicals production facilities (Kalisinska et al., 2012; Pirrone et al., 2010). Release of Hg into the environment has led to serious environmental problems globally (Counter et al., 2002; Campbell et al., 2008; Carneiro et al., 2014). Mercury has been detected in aquatic and terrestrial invertebrates, a variety of plants, and many higher organisms including humans. One of the problems and risks of Hg-induced adverse effects is of considerable ecological concern due to toxic manifestations in fish and wildlife (Scheuhammer et al., 2007; Wolfe et al., 1998; Sweet and Zelikoff, 2001; Burke et al., 2010)
Mercury (Hg) is a naturally occurring metal that is widespread in the environment (Gustin, 2003; Schuster et al., 2002; Mather and Pyle, 2004; United Nations Environment Programme [UNEP], 2013). This metal is one of the most toxic heavy metals emitted into the environment from several industrial process and other human activities, including pharmaceutical and chloralkali manufacturing industries (caustic soda production plants), electrical engineering, mining, agriculture, fossil-fuel-fired power plants, ore processing facilities, ferrous and nonferrous metals manufacturing facilities, incinerators for urban, medical, and industrial
Received 12 September 2014; accepted 20 September 2014. Address correspondence to Eisa Solgi, Department of Environment, Faculty of Natural Resources and Environment, Malayer University, PO Box 65719-65863, Hamedan, Iran. E-mail: [email protected] or [email protected] 342
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and the tendency to bioaccumulate and biomagnify in food webs and ecosystems (Burke et al., 2010; Zheng et al., 2101; Nichols et al., 1999; Hall et al., 1998). Smaller mammals such as mink, cats, dogs, and river otters appear to be more resistant to Hg than larger mammals (Eisler, 2006; Hinck et al., 2006). Eisler (2006) suggested that these differences are related to metabolism and possible higher Hg detoxification rates. For mammals, the main concern is Hg exposure levels during the early stages of pregnancy—the first trimester in humans (Ratcliffe et al., 1996; Marques et al., 2013). Terrestrial vertebrate organisms, including wild animals, absorb Hg via food, water, and air and through the skin (Kalisinska et al., 2012). On the other hand, when non-degradable pollutants such as Hg are released into the environment, these compounds are taken up and transferred through food chains and may accumulate in predators (Sanchez-Chardi et al., 2009) such as the brown bear (Ursus arctos). Wildlife that are predators and located at the top of food chain may be considered as bioindicators of ecosystems and environmental contamination by persistent toxic chemicals (Gufler et al., 1997; Dietz et al., 2000; Hoekstra et al., 2003; MacDonald et al., 2005; Lie et al., 2005; Oskam et al., 2004). One of the top predators with a typical food strategy is the brown bear (Ursus arctos) (Celechovska et al., 2006). Organic and inorganic pollutants were studied in the tissues of polar bear (Dietz et al., 2000; Muir et al., 1999; Hoekstra et al., 2003; Oskam et al 2004; Lie et al., 2005), but study in the case of the brown bear is limited to few investigations that reported heavy metals in brown bear tissues (Medvedev, 1999; Chudík and Maakovska, 1989; Zilincar et al., 1992; Celechovska et al., 2006). Hair is one of the noninvasive indicators commonly used in ecotoxicological studies to determine levels of heavy metal pollution and potential risk for adverse effects on humans and wildlife. The use of hair for in noninvasive monitoring of Hg in mammals or humans has been investigated (Marques et al., 2013; Ali Aldroobi et al., 2013; Wei et al., 2013; McHuron et al., 2012; McLean et al., 2009). Noninvasive
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sampling methods such as removal of feathers or hair for contaminant analysis are desirable in ecological monitoring programs that seek to minimize the impact of harvesting organs. These techniques enable investigators to obtain larger sample sizes without compromising ecological sustainability and to repeatedly sample individuals over time with limited interference to the organism. However, for noninvasive sampling methods to be most useful, concentrations of contaminants in these tissues need to accurately depict exposure history and concentrations of contaminants in tissue relevant to the organism’s health and reproductive success (Hopkins et al., 2005). The aim of this study was to utilize noninvasive tissue sampling for assessing Hg exposure in brown bear. Hair samples of mammals are considered to be reliable indicators of body burden of Hg (Johannesson et al., 1981; Hansen, 1981; Renzoni, 1989; Gerstenberger et al., 2006). Concentrations in hair reflect blood or body burden Hg during the period of hair growth (Sexton et al., 1978; Kershaw et al., 1980). Further, mammal fur and hairs are commonly used as target tissues to assess levels of a wide diversity of substances, including metals (Schramm, 1997; Rashed and Soltan, 2005). The highest levels of Hg occur in hair of mammals compared to other tissues; thus, hair has been used as a bioindicator of metal exposure (Newman et al., 2004) The U.S. Fish and Wildlife Service proposed a level of 1.1 µg/g fresh weight in hair and other tissues as indicative of an environmental Hg concern (Eisler, 1987). With regard to the stability of Hg in hair over time, it also may be possible to use hair samples from museum collections or other historical deposits to evaluate longer term changes in environmental exposure (Solgi et al., 2013). Thus, hair analysis of museum samples of mammals may be used retrospectively in assessment of Hg exposure in mammalian wildlife and provide baseline concentrations of metal. Historical records of hair Hg can therefore be obtained from museum specimens and compared with hair metal samples from recent years. This provides a means to examine trends in contamination rates, and to establish Hg
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concentrations that are representative of an earlier, less polluted time frame. The purpose of this study was to determine total Hg concentrations in the brown bear (Ursus arctos) by analysis of metal levels in hair from museum collections in Iran. Another objective of this investigation was to characterize the risk of Hg exposure in bears in several regions of Iran.
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MATERIAL AND METHODS Sample Collection and Analysis In this study, museums of 14 provinces were selected for sampling (Table 1). Thirty-five hair samples of brown bear from the museum’s collections were obtained (Figure 1). Hair specimens were removed with stainless-steel scissors by cutting them at the skin surface. Hairs were collected from various areas of the body to represent the body burden of Hg. Gender, age, decade, and information regarding the samples were also recorded. Hair samples were washed and homogenized before analyses. Then hair was washed using detergents and distilled water (rinsing), followed by final rinses with acetone. Then all of the hair samples were dried at room temperature. After drying, hair samples were cut into fine pieces like powder.
FIGURE 1. Geographical location of the sampling areas where brown bear was sampled.
Determination of Total Mercury Total mercury (Hg) concentration in the hair samples was measured by an advanced mercury analyzer (Leco AMA 254, USA). Results are reported on a dry weight (dw) basis as ng/g (ppb). Application of the method was reliable and convenient, such that this device did
TABLE 1. List of Provinces, Museums, and Decades for Hair Sampling of Brown Bear (Ursus arctos) Province
n
Name of museum
Year/decade
Ardebil East Azerbaijan Bushehr Charmaahl Esfahan Gilan Khorasan razavi Khozestan Lorestan Markazi Mazandaran
1 1 1 1 1 1 1 1 2 3 14
Pardisan Biodiversity Museum Iran Darabad Museum of Nature and Wildlife Bushehr Museum of Natural History Pardisan Biodiversity Museum Esfahan Museum of Natural History Gilan Museum of Natural History Zoological Museum, College of Agriculture, Tehran University shahid chamran university’s science and nature museum Lorestan Museum of Natural Science Arak Museum of Natural History Khoshkehdaran Museum, DOE babol,DOE Behshahr, Babolsar Natural Science Museum Wildlife Museum of Khojir and Sorkheh Hesar National Park
1996–2006 1996–2006 1996–2006 1996–2006 1986–1996 1996–2006 1986–1996 1996–2006 1986–1996 1996–2006 1986–1996, 1996–2006 1986–1996, 1996–2006 1986–1996 1986–1996
Tehran
2
Yazd Zanjan Total
1 5 35
Yazd Natural Science Museum Zanjan Museum of Natural History
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not require any previous pretreatment of the wet or dry samples and was placed directly in a nickel nacelle. The detector in the AMA 254 analyzer is a silicon ultraviolet (UV) diode operating at 254 nm, in a system of 2 measuring cells. The samples were analyzed at specified parameters of the cycle: 60/160/60, which means the time of drying (in seconds), time of decomposition (at 550◦ C), and waiting time for the measurement. In order to assess the analytical capability of the proposed methodology, accuracy of the total Hg analysis was checked by running three samples of standard reference materials (SRM), National Institute of Standard and Technology (NIST), (SRM 1633b, SRM 2709 and SRM 2711), and percent recovery varied between 94.8% and 105%. The limit of detection (LOD) of the instrument used (in AMA 254) was 0.001 µg/g of dry weight. Statistical Analysis Statistical analysis was carried out using SPSS Statistics version 17.5. In order to determine compliance with the expected normal distribution of results, the Shapiro–Wilk test (with p < .05) was used. Nonparametric tests (Kruskal–Wallis and Mann–Whitney Utest) were used for many of the analyses because the distributions were not normal, and when data were normally distributed parametric statistics including t-tests and one-way analysis of variance (ANOVA) were employed. Oneway analysis of variance was used to compare Hg levels in brown bears at four geographical locations. The statistical analysis was conducted at 95% confidence level and a p value < .05 was considered statistically significant.
RESULTS Total Hg was detected in all specimens from 1986 to 2006 and from different regions in Iran. Total Hg concentrations were calculated for all samples in nanograms per gram dry weight (ng/g dw). The Hg concentration ranged between 115.82 and 505.82 µg/kg for hair with mean 193.39 ± 14.25 µg/kg for
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all hair samples. Concentrations of total Hg found in brown bear hair in the 14 different provinces are presented in Table 2. The lowest metal concentrations were found in the East Azerbaijan province, while the highest levels were observed in the Khorasan Razavi province (Table 2). The order of Hg concentration in the provinces was as follows: Khorasan Razavi > Esfahan > Khozestan > Yazd > Lorestan > Charmahalva Bakhtiari > Bushehr > Mazandaran > Markazi > Tehran > Ardebil > Gilan > East Azerbaijan. To further investigate regional trends, differences were analyzed between Hg levels in bears from the west, versus those from south, north, and center. The means, standard deviation, standard errors, skewness, and kurtosis for different locations are presented in Table 3. In general, the mean Hg concentrations in hair of the brown bear, from highest to lowest, were as follow: south > center > north > west. In our study the highest levels of hair metal were found in the south. Mercury levels in bears from the north ranged from 129.64 to 409.79 ng/g with a mean of 187.9 ng/g. Mercury levels in bears from the south ranged from 172.79 to 236.29 ng/g with a mean of 206 .62 ng/g. Mercury levels in bears from the west ranged from 124.71 to 223.45 ng/g with a mean of 167.71 ng/g. Mercury levels in bears from the center ranged from 115.82 to 376.93 ng/g with a mean of 194.31 ng/g. Variations in hair Hg concentration in different location are presented in Figure 2. The trend of Hg levels for two decades 1986 and 1996 is shown in Figure 3. As illustrated in this figure, Hg concentrations decreased over in the past two decades. The mean value of metal in the decades of 1986 and 1996 fell from 234.84 to 165.76 ng/g, respectively. The Mann–Whitney U-test showed no significant difference between the two decades.
DISCUSSION In the present study, hair Hg concentrations ranged from 115.81 to 505.82 µg/kg.
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TABLE 2. Hair Mercury (ng/g) Concentration in Brown Bear From 14 Provinces of Iran Provinces Hg (ng/g) Provinces Hg (ng/g)
1 147.67 8 236.28
2 122.67 9 213.83
3 172.79 10 152.20
4 210.79 11 191.25
5 376.92 12 151.99
6 141.02 13 222.68
7 505.82 14 153.27
Note. Total samples: Min = 115.81, Mean = 193.39 Max = 505.82, Median = 162.18, SD = 84.32, SE = 14.25. Provinces: 1 Ardebil, 2 East Azerbaijan, 3 Bushehr, 4 Charmahalva Bakhtiari, 5 Esfahan, 6 Gilan, 7 Khorasan Razavi, 8 Khozestan, 9 Lorestan, 10 Markazi, 11 Mazandaran, 12 Tehran, 13 Yazd, 14 Zanjan.
Geographical location
n
Min
Max
Mean
SD
SE
Skewness
Kurtosis
North South West Center
15 3 8 7
129.64 172.79 124.71 115.82
409.79 236.29 223.45 376.93
187.90 206.62 167.71 194.31
73.97 31.95 32.97 88.13
19.09 18.44 11.65 33.31
2.27 −0.577 .644 1.81
5.49 — −.44 3.61
250
a
300
a
a
200
250
a
200 150
Hg(ng/g)
Hg(ng/g)
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TABLE 3. Variations in Mercury Concentration (ng/g) Based on Location in Hair of Brown Bear
100
150 100
50
50
0
0 North
South
West
Center
FIGURE 2. Outcome of comparison of average mercury concentration (mean ± SE) in brown bear hair between the different locations.
Sheffy and Amant (1982) suggested the range from 1 to 5 mg/kg was a normal background level of Hg in hair, indicating that comparison of these background values with our data showed that metal concentrations in brown bear hair were low. Based upon the U.S. Fish and Wildlife Service (USFWS) Hg concentration standard for ecosystem health is a maximum of 1.1 ppm Hg (Lord et al., 2002), levels of metal are lower than this value. Data indicate that Hg concentrations in brown bears are lower than those known to exert adverse physiological effects in wildlife experimentally dosed with methylmercury.
Decade 1986
Decade 1996
FIGURE 3. Trend of mercury concentration in two decades.
Various studies have been conducted in polar bears because this species feeds mainly on ringed and bearded seals. These seals are a significant accumulator of Hg with capability to accumulate metal between 27 to 420 ppm in liver (Eaton and Farant, 1982). Currently, only a handful of small studies have been conducted on Hg in brown bear. Our results are similar to those obtained by Celechovska et al. (2006) and Radova (2011), who determined heavy metals in tissues of brown bear. Celechovska et al. (2006) examined distribution of heavy metal including Hg in tissues of brown bear (Ursus arctos) living in the central Europe. The highest content of metal was found
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in the kidney (0.39 ± 0.25 mg/kg), whereas the lowest was observed in muscles (0.013 ± 0.011 mg/kg). In Croatia, Radova (2011) noted Hg in tissues of brown bears with the following distribution across tissues (median; range): muscle (0.002; 0.00008–0.018µg/g) < liver (0.034; 0.0001–0.198 µg/g) < kidney (0.238; 0.016–1.20 µg/g wet weight). Malvandi et al. (2010) reported concentration of Hg in hairs of golden jackal (Canis aureus) from the north of Iran at 187.3 ± 22.7 ng/g, while in the present study, metal levels in brown bear hairs from the north of Iran were 187.9 ± 19.09 ng/g. Although the species of brown bear is different from jackal, hair Hg levels in these two species are similar. This reflects the role of diet and habitat in accumulation of Hg where jackal and bear are both omnivorous mammals. It is noteworthy that museum specimens were found to be reliable indicators by Malvandi et al. (2010) for assessing environmental pollution using hair from the jackal. Several factors like location, age, and gender are confounding factors affecting differences in Hg concentrations in wild mammals (Wren, 1986). It is well documented that Hg bioaccumulation is correlated with long life span in mammals due to longer period of exposure and also as a consequence of low excretion rates. Because bears are omnivorous and eat a wide variety of foods, levels of Hg in the hair of bears from all areas were uniformly low (less than 1 ppm), but changes in metal levels in different provinces show that food habits of brown bear are different with regard to habitat. Food habit and habitat are two important factors that influence metal accumulation in bears. As an omnivore and top predator, the brown bear is especially susceptible to contamination by heavy metals from industry. It appears that differences in geographical locations in concentrations of total hair Hg in brown bears mainly reflect variation in overall metal burden in the environment and various prey species in their diet. In the southern areas due to the presence of various industries the highest mercury concentration was observed in hair of brown bears. Bocharova et al. (2013) demonstrated that total Hg concentrations in Arctic foxes
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(Vulpes lagopus) were more related to foraging strategies rather than variation in overall total Hg concentrations in the environment, and that high total Hg concentrations acquired predominantly through diet may represent a prominent risk for top predators. McGrew et al. (2014) studied Hg in Alaskan gray wolves, suggesting that cross-ecosystem utilization of food resources may contribute to increased Hg exposure, particularly in coastal populations. Atmospheric deposition is an important source of Hg to aquatic and terrestrial ecosystems and has global, regional, and local components. The Hg concentration was numerically lower in the period 1996–2006 compared to 1986–1996 (Table 1). In fact, decreasing trends were observed in the period 1986–2006, which may be mainly due to reduction of global Hg emissions. Ebinghaus et al. (2011) demonstrated decreasing trends in total gaseous Hg mercury in air at Mace Head, Ireland, from 1996 to 2009, in agreement with our results. There has been a considerable decrease in Hg concentrations between 1980 and 2002. A marked reduction at the Rörvik station on the Swedish West Coast was observed after 1990, which was attributed to cleaner energy production and reduced industrial emissions (Lövblad et al., 2004).
CONCLUSIONS Data indicated that hairs from mammals, particularly abundant omnivores, may be useful bioindicators of environmental quality over a long time period. Mercury concentrations in the hair of brown bears may be considered as a starting point to investigate the role of diet and habitat related to exposure of bears to residual contaminants. Monitoring studies in brown bears may be useful in order to verify whether the amount of contaminants in ecosystems poses a risk for both humans and animals. Our investigations of hair Hg levels revealed metal accumulation in brown bears in Iran, and indicate that hair may be used for monitoring metal concentrations in mammals. The Hg levels detected may not exert adverse effects in
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brown bears in different habitats in Iran, but may become problematic in future years as a result of increasingly growing industry and air pollution. From the present investigation it may be concluded that atmospheric deposition most probably contributes significantly to the heavy metal contaminant load in wildlife.
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Sanchez-Chardi, A., Ribeiro, C. A. O., and Nadal, J. 2009. Metals in liver and kidneys and the effects of chronic exposure to pyrite mine pollution in the shrew Crocidura russula inhabiting the protected wetland of Donana. Chemosphere 76: 387–394. Scheuhammer, A. M., Meyer, M. W., Sandheinrich, M. B., and Murray, M. W. 2007. Effects of environmental methylmercury on the health of wild birds, mammals, and fish. AMBIO 36: 12–18. Schramm, K. W. 1997. Hair, a matrix for noninvasive biomonitoring of organic chemicals in mammals. Bull. Environ. Contam. Toxicol. 59: 396–402. Schuster, P. F., Krabbenhoft, D. P., Naftz, D. L., Cecil, L. D., Olsom, M. L., and Dewild, J. F. 2002. Atmospheric mercury deposition during the last 270 years: A glacial ice core record of natural and anthropogenic sources. Environ. Sci. Technol. 36: 2303–2310. Sexton, D. J., Powell, K. E., Liddle, J., and Sinrek, A. 1978. A nonoccupational outbreak of inorganic mercury poisoning. Arch. Environ. Health 3: 186–191. Sheffy, T. B., and Amant, J. R. 1982. Mercury burdens in furbearers in Wisconsisn. J. Wildl. Manage. 46: 1117–1120. Solgi, E., Ghasempouri, S. M., and Esmaili-Sari, A. 2013. Mercury levels in the river otters (Lutra lutra) of Iran: Feasibility of back calculation for trace elements using old stuffed specimens. Ecopersia 1: 1–10. Sweet, L. I., and Zelikoff, J. T. 2001. Toxicology and immunotoxicology of mercury: A comparative review in fish and humans. J. Toxicol. Environ. Health B 4: 161–205. United Nations Environment Programme. 2013. Global mercury assessment 2013, Sources, emissions, releases and environmental transport. Geneva, Switzerland: UNEP Chemicals Branch. Wei, B., Yonghua, L., Hairong, L., Jiangping, Y., Bixiong, Y., and Liang, T. 2013. Rare earth elements in human hair from a mining area of China. Ecotoxicol. Environ. Safety 96: 118–123. Wolfe, M. F., Schwarzbach, S., and Sulaiman, R. A. 1998. Effects of mercury on wildlife:
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Journal of Toxicology and Environmental Health, Part A: Current Issues Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/uteh20
Application of Brown Bear (Ursus arctos) Records for Retrospective Assessment of Mercury a
b
Eisa Solgi & Seyed Mahmoud Ghasempouri a
Department of Environment, Faculty of Natural Resources and Environment, Malayer University, Hamedan, Iran b
Department of Environment, Faculty of Natural Resources and Marine Science, Tarbiat Modares University, Noor, Mazandaran, Iran Published online: 03 Mar 2015.
Click for updates To cite this article: Eisa Solgi & Seyed Mahmoud Ghasempouri (2015) Application of Brown Bear (Ursus arctos) Records for Retrospective Assessment of Mercury, Journal of Toxicology and Environmental Health, Part A: Current Issues, 78:5, 342-351, DOI: 10.1080/15287394.2014.968816 To link to this article: http://dx.doi.org/10.1080/15287394.2014.968816
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Journal of Toxicology and Environmental Health, Part A, 78:342–351, 2015 Copyright © Taylor & Francis Group, LLC ISSN: 1528-7394 print / 1087-2620 online DOI: 10.1080/15287394.2014.968816
APPLICATION OF BROWN BEAR (Ursus arctos) RECORDS FOR RETROSPECTIVE ASSESSMENT OF MERCURY Eisa Solgi1, Seyed Mahmoud Ghasempouri2 1
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Department of Environment, Faculty of Natural Resources and Environment, Malayer University, Hamedan, Iran 2 Department of Environment, Faculty of Natural Resources and Marine Science, Tarbiat Modares University, Noor, Mazandaran, Iran Because mercury (Hg) is released into the atmosphere, wildlife living in habitats located far from point sources of metal may still be at risk. Mercury accumulation, previously considered a risk for aquatic ecosystems, is also found in many wildlife terrestrial species. The aim of the present study was to examine total Hg concentrations in the brown bear (Ursus arctos) by measurement of metal in hair from museum collections in Iran. Another objective of this investigation was to characterize the risk of Hg exposure in bears in several parts of Iran. Brown bear (Ursus arctos) hair samples (n = 35) were collected from 14 provinces in Iran for analysis of Hg contamination, performed using an advanced mercury analyzer (model Leco 254 AMA, USA) according to ASTM standard D-6722. Total Hg levels in Iranian bears from all areas ranged from 115.81 to 505.82 µg/kg, with a mean of 193.39 ng/g. Mercury concentrations in brown bear hair from different provinces in Iran were as follows in descending order: Khorasan Razavi > Esfahan > Khozestan > Yazd > Lorestan > Charmahalva Bakhtiari > Bushehr > Mazandaran > Markazi > Tehran > Ardebil > Gilan > East Azerbaijan. The highest content of Hg was found in the south (206.62 ± 31.95 ng/g), whereas the lowest levels were detected in the west (167.71 ± 32.97 ng/g). Overall total Hg content in bear hair was below harmful levels for this species. A decreasing trend was noted in the period 1986–2006, which may be mainly due to reduction of global Hg emissions. Data suggest that food habits and habitat are two important factors that influence Hg accumulation in bears.
wastes, cement plants, and chemicals production facilities (Kalisinska et al., 2012; Pirrone et al., 2010). Release of Hg into the environment has led to serious environmental problems globally (Counter et al., 2002; Campbell et al., 2008; Carneiro et al., 2014). Mercury has been detected in aquatic and terrestrial invertebrates, a variety of plants, and many higher organisms including humans. One of the problems and risks of Hg-induced adverse effects is of considerable ecological concern due to toxic manifestations in fish and wildlife (Scheuhammer et al., 2007; Wolfe et al., 1998; Sweet and Zelikoff, 2001; Burke et al., 2010)
Mercury (Hg) is a naturally occurring metal that is widespread in the environment (Gustin, 2003; Schuster et al., 2002; Mather and Pyle, 2004; United Nations Environment Programme [UNEP], 2013). This metal is one of the most toxic heavy metals emitted into the environment from several industrial process and other human activities, including pharmaceutical and chloralkali manufacturing industries (caustic soda production plants), electrical engineering, mining, agriculture, fossil-fuel-fired power plants, ore processing facilities, ferrous and nonferrous metals manufacturing facilities, incinerators for urban, medical, and industrial
Received 12 September 2014; accepted 20 September 2014. Address correspondence to Eisa Solgi, Department of Environment, Faculty of Natural Resources and Environment, Malayer University, PO Box 65719-65863, Hamedan, Iran. E-mail: [email protected] or [email protected] 342
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and the tendency to bioaccumulate and biomagnify in food webs and ecosystems (Burke et al., 2010; Zheng et al., 2101; Nichols et al., 1999; Hall et al., 1998). Smaller mammals such as mink, cats, dogs, and river otters appear to be more resistant to Hg than larger mammals (Eisler, 2006; Hinck et al., 2006). Eisler (2006) suggested that these differences are related to metabolism and possible higher Hg detoxification rates. For mammals, the main concern is Hg exposure levels during the early stages of pregnancy—the first trimester in humans (Ratcliffe et al., 1996; Marques et al., 2013). Terrestrial vertebrate organisms, including wild animals, absorb Hg via food, water, and air and through the skin (Kalisinska et al., 2012). On the other hand, when non-degradable pollutants such as Hg are released into the environment, these compounds are taken up and transferred through food chains and may accumulate in predators (Sanchez-Chardi et al., 2009) such as the brown bear (Ursus arctos). Wildlife that are predators and located at the top of food chain may be considered as bioindicators of ecosystems and environmental contamination by persistent toxic chemicals (Gufler et al., 1997; Dietz et al., 2000; Hoekstra et al., 2003; MacDonald et al., 2005; Lie et al., 2005; Oskam et al., 2004). One of the top predators with a typical food strategy is the brown bear (Ursus arctos) (Celechovska et al., 2006). Organic and inorganic pollutants were studied in the tissues of polar bear (Dietz et al., 2000; Muir et al., 1999; Hoekstra et al., 2003; Oskam et al 2004; Lie et al., 2005), but study in the case of the brown bear is limited to few investigations that reported heavy metals in brown bear tissues (Medvedev, 1999; Chudík and Maakovska, 1989; Zilincar et al., 1992; Celechovska et al., 2006). Hair is one of the noninvasive indicators commonly used in ecotoxicological studies to determine levels of heavy metal pollution and potential risk for adverse effects on humans and wildlife. The use of hair for in noninvasive monitoring of Hg in mammals or humans has been investigated (Marques et al., 2013; Ali Aldroobi et al., 2013; Wei et al., 2013; McHuron et al., 2012; McLean et al., 2009). Noninvasive
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sampling methods such as removal of feathers or hair for contaminant analysis are desirable in ecological monitoring programs that seek to minimize the impact of harvesting organs. These techniques enable investigators to obtain larger sample sizes without compromising ecological sustainability and to repeatedly sample individuals over time with limited interference to the organism. However, for noninvasive sampling methods to be most useful, concentrations of contaminants in these tissues need to accurately depict exposure history and concentrations of contaminants in tissue relevant to the organism’s health and reproductive success (Hopkins et al., 2005). The aim of this study was to utilize noninvasive tissue sampling for assessing Hg exposure in brown bear. Hair samples of mammals are considered to be reliable indicators of body burden of Hg (Johannesson et al., 1981; Hansen, 1981; Renzoni, 1989; Gerstenberger et al., 2006). Concentrations in hair reflect blood or body burden Hg during the period of hair growth (Sexton et al., 1978; Kershaw et al., 1980). Further, mammal fur and hairs are commonly used as target tissues to assess levels of a wide diversity of substances, including metals (Schramm, 1997; Rashed and Soltan, 2005). The highest levels of Hg occur in hair of mammals compared to other tissues; thus, hair has been used as a bioindicator of metal exposure (Newman et al., 2004) The U.S. Fish and Wildlife Service proposed a level of 1.1 µg/g fresh weight in hair and other tissues as indicative of an environmental Hg concern (Eisler, 1987). With regard to the stability of Hg in hair over time, it also may be possible to use hair samples from museum collections or other historical deposits to evaluate longer term changes in environmental exposure (Solgi et al., 2013). Thus, hair analysis of museum samples of mammals may be used retrospectively in assessment of Hg exposure in mammalian wildlife and provide baseline concentrations of metal. Historical records of hair Hg can therefore be obtained from museum specimens and compared with hair metal samples from recent years. This provides a means to examine trends in contamination rates, and to establish Hg
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concentrations that are representative of an earlier, less polluted time frame. The purpose of this study was to determine total Hg concentrations in the brown bear (Ursus arctos) by analysis of metal levels in hair from museum collections in Iran. Another objective of this investigation was to characterize the risk of Hg exposure in bears in several regions of Iran.
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MATERIAL AND METHODS Sample Collection and Analysis In this study, museums of 14 provinces were selected for sampling (Table 1). Thirty-five hair samples of brown bear from the museum’s collections were obtained (Figure 1). Hair specimens were removed with stainless-steel scissors by cutting them at the skin surface. Hairs were collected from various areas of the body to represent the body burden of Hg. Gender, age, decade, and information regarding the samples were also recorded. Hair samples were washed and homogenized before analyses. Then hair was washed using detergents and distilled water (rinsing), followed by final rinses with acetone. Then all of the hair samples were dried at room temperature. After drying, hair samples were cut into fine pieces like powder.
FIGURE 1. Geographical location of the sampling areas where brown bear was sampled.
Determination of Total Mercury Total mercury (Hg) concentration in the hair samples was measured by an advanced mercury analyzer (Leco AMA 254, USA). Results are reported on a dry weight (dw) basis as ng/g (ppb). Application of the method was reliable and convenient, such that this device did
TABLE 1. List of Provinces, Museums, and Decades for Hair Sampling of Brown Bear (Ursus arctos) Province
n
Name of museum
Year/decade
Ardebil East Azerbaijan Bushehr Charmaahl Esfahan Gilan Khorasan razavi Khozestan Lorestan Markazi Mazandaran
1 1 1 1 1 1 1 1 2 3 14
Pardisan Biodiversity Museum Iran Darabad Museum of Nature and Wildlife Bushehr Museum of Natural History Pardisan Biodiversity Museum Esfahan Museum of Natural History Gilan Museum of Natural History Zoological Museum, College of Agriculture, Tehran University shahid chamran university’s science and nature museum Lorestan Museum of Natural Science Arak Museum of Natural History Khoshkehdaran Museum, DOE babol,DOE Behshahr, Babolsar Natural Science Museum Wildlife Museum of Khojir and Sorkheh Hesar National Park
1996–2006 1996–2006 1996–2006 1996–2006 1986–1996 1996–2006 1986–1996 1996–2006 1986–1996 1996–2006 1986–1996, 1996–2006 1986–1996, 1996–2006 1986–1996 1986–1996
Tehran
2
Yazd Zanjan Total
1 5 35
Yazd Natural Science Museum Zanjan Museum of Natural History
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not require any previous pretreatment of the wet or dry samples and was placed directly in a nickel nacelle. The detector in the AMA 254 analyzer is a silicon ultraviolet (UV) diode operating at 254 nm, in a system of 2 measuring cells. The samples were analyzed at specified parameters of the cycle: 60/160/60, which means the time of drying (in seconds), time of decomposition (at 550◦ C), and waiting time for the measurement. In order to assess the analytical capability of the proposed methodology, accuracy of the total Hg analysis was checked by running three samples of standard reference materials (SRM), National Institute of Standard and Technology (NIST), (SRM 1633b, SRM 2709 and SRM 2711), and percent recovery varied between 94.8% and 105%. The limit of detection (LOD) of the instrument used (in AMA 254) was 0.001 µg/g of dry weight. Statistical Analysis Statistical analysis was carried out using SPSS Statistics version 17.5. In order to determine compliance with the expected normal distribution of results, the Shapiro–Wilk test (with p < .05) was used. Nonparametric tests (Kruskal–Wallis and Mann–Whitney Utest) were used for many of the analyses because the distributions were not normal, and when data were normally distributed parametric statistics including t-tests and one-way analysis of variance (ANOVA) were employed. Oneway analysis of variance was used to compare Hg levels in brown bears at four geographical locations. The statistical analysis was conducted at 95% confidence level and a p value < .05 was considered statistically significant.
RESULTS Total Hg was detected in all specimens from 1986 to 2006 and from different regions in Iran. Total Hg concentrations were calculated for all samples in nanograms per gram dry weight (ng/g dw). The Hg concentration ranged between 115.82 and 505.82 µg/kg for hair with mean 193.39 ± 14.25 µg/kg for
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all hair samples. Concentrations of total Hg found in brown bear hair in the 14 different provinces are presented in Table 2. The lowest metal concentrations were found in the East Azerbaijan province, while the highest levels were observed in the Khorasan Razavi province (Table 2). The order of Hg concentration in the provinces was as follows: Khorasan Razavi > Esfahan > Khozestan > Yazd > Lorestan > Charmahalva Bakhtiari > Bushehr > Mazandaran > Markazi > Tehran > Ardebil > Gilan > East Azerbaijan. To further investigate regional trends, differences were analyzed between Hg levels in bears from the west, versus those from south, north, and center. The means, standard deviation, standard errors, skewness, and kurtosis for different locations are presented in Table 3. In general, the mean Hg concentrations in hair of the brown bear, from highest to lowest, were as follow: south > center > north > west. In our study the highest levels of hair metal were found in the south. Mercury levels in bears from the north ranged from 129.64 to 409.79 ng/g with a mean of 187.9 ng/g. Mercury levels in bears from the south ranged from 172.79 to 236.29 ng/g with a mean of 206 .62 ng/g. Mercury levels in bears from the west ranged from 124.71 to 223.45 ng/g with a mean of 167.71 ng/g. Mercury levels in bears from the center ranged from 115.82 to 376.93 ng/g with a mean of 194.31 ng/g. Variations in hair Hg concentration in different location are presented in Figure 2. The trend of Hg levels for two decades 1986 and 1996 is shown in Figure 3. As illustrated in this figure, Hg concentrations decreased over in the past two decades. The mean value of metal in the decades of 1986 and 1996 fell from 234.84 to 165.76 ng/g, respectively. The Mann–Whitney U-test showed no significant difference between the two decades.
DISCUSSION In the present study, hair Hg concentrations ranged from 115.81 to 505.82 µg/kg.
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TABLE 2. Hair Mercury (ng/g) Concentration in Brown Bear From 14 Provinces of Iran Provinces Hg (ng/g) Provinces Hg (ng/g)
1 147.67 8 236.28
2 122.67 9 213.83
3 172.79 10 152.20
4 210.79 11 191.25
5 376.92 12 151.99
6 141.02 13 222.68
7 505.82 14 153.27
Note. Total samples: Min = 115.81, Mean = 193.39 Max = 505.82, Median = 162.18, SD = 84.32, SE = 14.25. Provinces: 1 Ardebil, 2 East Azerbaijan, 3 Bushehr, 4 Charmahalva Bakhtiari, 5 Esfahan, 6 Gilan, 7 Khorasan Razavi, 8 Khozestan, 9 Lorestan, 10 Markazi, 11 Mazandaran, 12 Tehran, 13 Yazd, 14 Zanjan.
Geographical location
n
Min
Max
Mean
SD
SE
Skewness
Kurtosis
North South West Center
15 3 8 7
129.64 172.79 124.71 115.82
409.79 236.29 223.45 376.93
187.90 206.62 167.71 194.31
73.97 31.95 32.97 88.13
19.09 18.44 11.65 33.31
2.27 −0.577 .644 1.81
5.49 — −.44 3.61
250
a
300
a
a
200
250
a
200 150
Hg(ng/g)
Hg(ng/g)
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TABLE 3. Variations in Mercury Concentration (ng/g) Based on Location in Hair of Brown Bear
100
150 100
50
50
0
0 North
South
West
Center
FIGURE 2. Outcome of comparison of average mercury concentration (mean ± SE) in brown bear hair between the different locations.
Sheffy and Amant (1982) suggested the range from 1 to 5 mg/kg was a normal background level of Hg in hair, indicating that comparison of these background values with our data showed that metal concentrations in brown bear hair were low. Based upon the U.S. Fish and Wildlife Service (USFWS) Hg concentration standard for ecosystem health is a maximum of 1.1 ppm Hg (Lord et al., 2002), levels of metal are lower than this value. Data indicate that Hg concentrations in brown bears are lower than those known to exert adverse physiological effects in wildlife experimentally dosed with methylmercury.
Decade 1986
Decade 1996
FIGURE 3. Trend of mercury concentration in two decades.
Various studies have been conducted in polar bears because this species feeds mainly on ringed and bearded seals. These seals are a significant accumulator of Hg with capability to accumulate metal between 27 to 420 ppm in liver (Eaton and Farant, 1982). Currently, only a handful of small studies have been conducted on Hg in brown bear. Our results are similar to those obtained by Celechovska et al. (2006) and Radova (2011), who determined heavy metals in tissues of brown bear. Celechovska et al. (2006) examined distribution of heavy metal including Hg in tissues of brown bear (Ursus arctos) living in the central Europe. The highest content of metal was found
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in the kidney (0.39 ± 0.25 mg/kg), whereas the lowest was observed in muscles (0.013 ± 0.011 mg/kg). In Croatia, Radova (2011) noted Hg in tissues of brown bears with the following distribution across tissues (median; range): muscle (0.002; 0.00008–0.018µg/g) < liver (0.034; 0.0001–0.198 µg/g) < kidney (0.238; 0.016–1.20 µg/g wet weight). Malvandi et al. (2010) reported concentration of Hg in hairs of golden jackal (Canis aureus) from the north of Iran at 187.3 ± 22.7 ng/g, while in the present study, metal levels in brown bear hairs from the north of Iran were 187.9 ± 19.09 ng/g. Although the species of brown bear is different from jackal, hair Hg levels in these two species are similar. This reflects the role of diet and habitat in accumulation of Hg where jackal and bear are both omnivorous mammals. It is noteworthy that museum specimens were found to be reliable indicators by Malvandi et al. (2010) for assessing environmental pollution using hair from the jackal. Several factors like location, age, and gender are confounding factors affecting differences in Hg concentrations in wild mammals (Wren, 1986). It is well documented that Hg bioaccumulation is correlated with long life span in mammals due to longer period of exposure and also as a consequence of low excretion rates. Because bears are omnivorous and eat a wide variety of foods, levels of Hg in the hair of bears from all areas were uniformly low (less than 1 ppm), but changes in metal levels in different provinces show that food habits of brown bear are different with regard to habitat. Food habit and habitat are two important factors that influence metal accumulation in bears. As an omnivore and top predator, the brown bear is especially susceptible to contamination by heavy metals from industry. It appears that differences in geographical locations in concentrations of total hair Hg in brown bears mainly reflect variation in overall metal burden in the environment and various prey species in their diet. In the southern areas due to the presence of various industries the highest mercury concentration was observed in hair of brown bears. Bocharova et al. (2013) demonstrated that total Hg concentrations in Arctic foxes
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(Vulpes lagopus) were more related to foraging strategies rather than variation in overall total Hg concentrations in the environment, and that high total Hg concentrations acquired predominantly through diet may represent a prominent risk for top predators. McGrew et al. (2014) studied Hg in Alaskan gray wolves, suggesting that cross-ecosystem utilization of food resources may contribute to increased Hg exposure, particularly in coastal populations. Atmospheric deposition is an important source of Hg to aquatic and terrestrial ecosystems and has global, regional, and local components. The Hg concentration was numerically lower in the period 1996–2006 compared to 1986–1996 (Table 1). In fact, decreasing trends were observed in the period 1986–2006, which may be mainly due to reduction of global Hg emissions. Ebinghaus et al. (2011) demonstrated decreasing trends in total gaseous Hg mercury in air at Mace Head, Ireland, from 1996 to 2009, in agreement with our results. There has been a considerable decrease in Hg concentrations between 1980 and 2002. A marked reduction at the Rörvik station on the Swedish West Coast was observed after 1990, which was attributed to cleaner energy production and reduced industrial emissions (Lövblad et al., 2004).
CONCLUSIONS Data indicated that hairs from mammals, particularly abundant omnivores, may be useful bioindicators of environmental quality over a long time period. Mercury concentrations in the hair of brown bears may be considered as a starting point to investigate the role of diet and habitat related to exposure of bears to residual contaminants. Monitoring studies in brown bears may be useful in order to verify whether the amount of contaminants in ecosystems poses a risk for both humans and animals. Our investigations of hair Hg levels revealed metal accumulation in brown bears in Iran, and indicate that hair may be used for monitoring metal concentrations in mammals. The Hg levels detected may not exert adverse effects in
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brown bears in different habitats in Iran, but may become problematic in future years as a result of increasingly growing industry and air pollution. From the present investigation it may be concluded that atmospheric deposition most probably contributes significantly to the heavy metal contaminant load in wildlife.
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