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Mercury Contamination of Cattle in Artisanal and Small-Scale Gold Mining in Bombana, Southeast Sulawesi, Indonesia

Graduate School of Science and Engineering, Ehime University, 2-5 Bunkyo-cho, Matsuyama, Ehime Prefecture 790-8577, Japan
Makassar School of Health Science (Sekolah Tinggi Ilmu Kesehatan Makassar), Jl. Maccini Raya No. 197, Makassar 90231, Indonesia
Faculty of Collaborative Regional Innovation, Ehime University, 3 Bunkyo-cho, Matsuyama, Ehime Prefecture 790-8577, Japan
Cyclotron Research Centre, Iwate Medical University, 348-58 Tomegamori, Takizawa, Iwate 020-0173, Japan
Author to whom correspondence should be addressed.
Geosciences 2017, 7(4), 133;
Submission received: 2 August 2017 / Revised: 30 November 2017 / Accepted: 11 December 2017 / Published: 14 December 2017
(This article belongs to the Special Issue Urban Environmental and Medical Geochemistry)


The industrial mining sector is one of the main contributors to environmental damage and toxic metal pollution, although some contamination originates from natural geological sources. Due to their position at the top of the food chain, cattle tend to bioaccumulate mercury (Hg) in their bodies. We used analyses of cattle hair samples to investigate Hg contamination in cattle farmed within and outside of an artisanal and small-scale gold-mining area in Bombana, Southeast Sulawesi, Indonesia. We also examined the factors that might have influenced the toxicity, such as the environmental conditions, sex, and age of the cattle. A total of 63 hair samples were analyzed by particle-induced X-ray emission spectrometry. The mean Hg concentration was significantly higher in hair from cattle farmed within the artisanal and small-scale gold mining area (11.44 μg/g hair) than in those farmed outside the area (2.89 μg/g hair, p < 0.05). A possible cause of this is contamination by mercury persistent in terrestrial food chain. The results indicates that the level of toxic metals such as Hg need to be controlled in food sources to protect human health, especially in Bombana, Indonesia.

1. Introduction

Although the industrial and agricultural sectors are largely responsible for environmental degradation and toxic metal pollution, some contamination comes from natural geological sources, and these can be evaluated through geochemical factor analysis [1,2,3]. Mercury is a highly toxic element, and is released into the environment as metallic Hg [4,5]. Up to ~80% is derived from human activities, such as burning fossil fuels, mining, smelting, and burning waste; with the remainder primarily from volcanoes and forest fires [6,7,8]. The artisanal and small-scale gold mining (ASGM) sector, as informal (illegal) mining, is responsible for 37% of all anthropogenic mercury emissions in the environment. Mercury-based gold extraction has resulted in increased levels of various forms of natural mercury (Hg), such as elemental, organic, and inorganic Hg. As a persistent contaminant, Hg is transported easily and biomagnifies through the food web without noticeable biological function [9], causing mortality, reproductive failure, and other health effects in animals [10,11]. Methylmercury tends to accumulate and biomagnify in the bodies of herbivores at the second trophic level of the terrestrial food chain [12,13].
Bioaccumulation of metals in the food chain process occurs in all animals, including food animals such as fish and cattle, and also in humans [2,14]. Diet in large mammals is the main route for metal accumulation, causing heavy metal accumulation in the kidneys, liver, bones, hair, and blood of these mammals. Cows, as large mammals, often swallow grass or other contaminated vegetation, drinking water, and small amounts of contaminated soil, although there is a possibility of exposure to metals through inhalation or treatment. The presence of Hg in meat and meat products is a major concern for public health and food security itself, causing widespread concern about public health [3]. Therefore, the levels of these toxic metals in foodstuffs need to be controlled, and this is of particular interest in Bombana.
In general, the toxic effect of Hg depends on the form and dose of Hg, the exposure duration, and the ingestion route. Exposure to Hg has been found to be toxic to both humans and animals [6]. There are similarities and differences in the toxic effects of the various forms of Hg [15,16]. Organic Hg is the more toxic form, and causes poisoning if ingested [17]. The major targets of toxicity from inorganic and organic Hg are the kidneys and the central nervous system, respectively. The clinical signs of Hg poisoning in cattle vary greatly, and include ataxia, neuromuscular incoordination, and renal failure, followed by convulsions and a moribund state [18,19].
Some literature has discussed the accumulation of heavy metals in large mammals, including cattle [20]. Large mammals that are on the second trophic level of the terrestrial food chain ingest contaminated vegetation mixed with small amounts of soil, or contaminated drinking water [21]. However, metal mobility and its availability in the soil determine the risk of metals entering the food chain [22]. As a hypothesis, a possible cause of this is contamination by mercury persistent in terrestrial food chain. This may become a food safety issue in the future, as long-term consumption of contaminated beef can cause Hg poisoning in humans.
There is concern that feed for livestock is contaminated locally by Hg-based gold processing activities, with implications for toxicity in cattle herds. To date, however, there is no information regarding the Hg concentration in livestock in Bombana, or in any other region of Sulawesi. In this preliminary study, we collected samples of hair to investigate the level of Hg contamination in cattle from two regions of Bombana. The three specific objectives of our study were (i) to measure the total Hg concentrations in hair from cattle, (ii) to investigate whether Hg residues varied with the age or sex of the cattle, and (iii) to determine whether the gold mining industry was associated with increased levels of total Hg in cattle.

2. Materials and Methods

2.1. Study Area and Geological Background

Bombana has two ASGM sites that have expanded progressively over the past ten years [23]. Secondary gold deposits can be found in the Bombana gold mining sites. This type, discovered in the form of alluvial gold, is formed by obtaining gold through a natural process. The oxidation process influences the circulation of water and leads to the disintegration of gold ore constituents. In this location, the alluvial type contains gold granules of excessive size, spread over an area only a few meters wide, are relatively shallowly deposited, and which are explored using large-capacity equipment. The sediments formed in ASGM include mica schist, glaucophane schist, amphibole schist, chlorite schist, jasperoidal chert, genesis schist, marble, and metalimestone. Significant levels of gold production create high levels of income for local miners, and has encouraged the rapid development of the small-scale gold mining industry in a short time.
The number of cattle in the Bombana area increased from 46,686 in 2014 to 54,029 in 2016, and they are currently the most important agricultural animal in this region. Bombana is the largest beef-producing center in Sulawesi, and accounts for about 70% of Sulawesi’s total production. Altogether, there are about 5000 head of cattle in the sub-districts of Rarowatu and North Rarowatu, which have been the focus of the gold mining industry since 2008. In Bombana ASGM areas, cattle are directly exposed to Hg vapor, because they are farmed close to sites where gold is mined and refined. In addition, waste from the mines can contaminate soil, water bodies, and animal feed.
The study was conducted in the Bombana Regency of Southeast Sulawesi, Indonesia (Figure 1), where agriculture is dominated by cattle ranching. We performed sampling in the Rarowatu sub-district, as it contained artisanal and small-scale gold mining (ASGM) development areas that had probably been contaminated with heavy metals, particularly mercury. The sampling area was expanded to the North Rarowatu sub-district to cover non-ASGM areas as a comparison.

2.2. Sample Collection

To obtain cattle hair for analysis of total mercury (tHg) levels, we collected hair samples from similar numbers of male and female cattle aged 1–15 years, from cattle farmed in the two sampling areas, over the period from August 2016 to March 2017 (Figure 2). We also attempted to determine the factors influencing the toxic levels of Hg in the samples. Hair samples were taken from cows representing each of the colonies using a non-random approach. The selection of each territory was based on the factors of distance and permitted access from the local community. The cows live in groups and move within a 3 km2 range for food. The sample distribution within the ASGM area was denser than outside of ASGM site. The landscape at the ASGM sites was dominated by tropical savanna hill, while outside the ASGM sites, landscape conditions were widely distributed among rivers, forest edges, and rice field locations. The total area of sampling was about 130 km2.

2.3. Analytical Method

The samples were shaken with Milli-Q water (18.2 MΩ/cm) in an ultrasonic cleaning bath (Sharp) for 5 min to remove dust, dirt, bacteria, and other contaminants. The samples were then dried with sterile paper on a clean glass plate for 10 min. The dried samples were stirred in acetone solution (Wako Pure Chemical Industries, Ltd., Osaka, Japan) for 5 min to remove any organic material that was not water soluble [6,11]. The samples were then washed again with Milli-Q water and dried using sterile tissue at room temperature. Several strands of hair were randomly selected from each dried sample and cut into sections that included either the root or the end of the strand. About eight hair samples were attached parallel to the sample holder during preparation of the target. The Environmentally Certified Reference Materials (CRMs) from the National Institute for Environmental Studies was prepared for use in evaluation of accuracy of tHg of animal hair. The samples were analyzed by particle-induced X-ray emission (PIXE) at the Cyclotron Research Center, Iwate Technical University, Japan, using a proton energy beam of 2.5–3 MeV. In this method, the X-ray emissions from the sample that pass through the target area were detected by a Si (Li) detector. Low-energy X-rays were attenuated by a 300-pm Mylar Mixer filter. Rays of uniform density were combined to have a diameter of 6 mm with a thick nickel foil and a diffuser in a graphite collimator system. The samples were placed on the target rectangle at an angle of ~35° to the horizontal beam axis.

2.4. Data Analysis

The data sets both within and without the ASGM site were not normally distributed, but had the same variance. We used the Mann-Whitney U test to identify differences in Hg concentrations in hair from cattle in Rarowatu and North Rarowatu, with reference to sex, age, and sample site. Differences were considered significant for p values < 0.05. In all statistical analyses, Paleontological Statistic (PAST) Ver. 3.17 and IBM SPSS Statistic 21 Ver. 21.0 [24] were utilized.

3. Results

3.1. Laboratory Data

The analytical results are listed in Table 1. Of the 63 samples of hair collected, 34 were taken from cattle farmed within the two ASGM areas, and 29 were from cattle farmed outside the ASGM areas (total female, n = 42; male, n = 21). Fewer males were sampled, because they are farmed in smaller numbers than females. There was no statistically significant relationship between sex and sampling location (p > 0.05). Minimum and maximum ages were the same in both of the sampling sites, inside and outside the ASGM area, and the mean and median ages were higher in the two ASGM sites than outside the sites. Age was significantly different between the two sampling sites (p < 0.05).

3.2. Source of Exposure

There was a statistically significantly difference in Hg concentration among hair samples from inside and outside ASGM area with p < 0.05 (Figure 3). PIXE analysis revealed higher mean and median Hg levels in the hair of animals farmed within the ASGM site than in those farmed outside these areas.
The mean Hg concentration in hair from ASGM areas (n = 34; 11.44 μg Hg/g hair) was almost three times that in hair from outside the ASGM areas (n = 29; 2.89 μg Hg/g hair). The Mann-Whitney U test revealed a statistically significant difference in Hg concentration in hair from inside and outside the ASGM sites (p < 0.05) (Figure 4). The values for the two ASGM sites combined were as follows: range, 0.15–36.08 μg/g; mean, 7.60 μg/g; standard deviation, 8.33 μg/g.
There was a statistically significant difference in the age of cattle from inside and outside the ASGM area, with p < 0.05 (Table 1). Comparison of the rate of Hg accumulation according to age differences between cattle farmed inside and outside the ASGM areas. In hair from both sampling areas, there was a positive correlation between Hg concentration and age (Figure 5).

3.3. Sex and Hormonal Status

There was no difference in Hg accumulation in cattle with respect to the sex of the animal (Figure 6A). The PIXE analytical method showed that the mean Hg concentration was higher in females than in males (8.21 and 6.10 μg/g, respectively), but the difference was not statistically significant (Mann-Whitney U test, p > 0.05; Table 1). The hair concentration was higher in the ASGM areas than in these areas, although significant differences were found in males (Mann-Whitney U test, p < 0.05; Table 1). Similarly, in the females, Hg concentration was higher in the ASGM area, but there was no significant difference (Figure 6B).

4. Discussion

The response of an animal population to a certain amount of toxicant may differ among individuals, because various factors can modulate the overall toxic response [25,26]. Drugs and toxins may be substituted in some kinetic or dynamic interactions when binding to plasma proteins or receptors at the active site of the enzyme involved in biotransformation [27,28]. The main factors affecting chemical toxicity in individuals and in populations are breed, age, sex, pathophysiological events, diet composition, environmental conditions, the source, and route of exposure [26]. Here, we examine the influence of environmental conditions, age, maturity, sex, and hormonal status.

4.1. Environmental Condition

Previous studies have shown that miners who work in this area have been contaminated with heavy metals, having hair Hg levels as high as 12.82 μg/g [23]. During the gold purification process, gold particles are separated from river sediments, and are extracted from soil ore by washing and filtering; they are then added to liquid Hg to form an amalgam, which is then fed into a retort or a heated distillation vessel, vaporizing the Hg and leaving the gold [29,30]. Mercury is a critical component of the liquid metal capture process in ASGM; however, some of the Hg is lost during this process [31,32,33] and contaminates animals that are farmed nearby [34,35].

4.2. Age and Maturity

Because Hg is thought to bioaccumulate, the concentration of Hg tends to increase with continued exposure, and thus the age of the animal [20]. This finding indicates that exposure to the residue of gold combustion is linked to Hg accumulation in terrestrial food chains. Younger humans and animals are generally more sensitive to the effects of chemicals than are older humans and animals, for reasons that include differences in absorption rate, plasma protein binding, distribution, biotransformation, and excretion [36].
Previous animal studies have reported an increasing sensitivity to toxins with age, and that the effect was more pronounced in food-producing species that have a long life cycle [37,38,39]. Pharmacokinetic conditions in groups such as older people, different ethnic groups, and pregnant women will have different pathological effects (e.g., renal and hepatic insufficiency, cardiac dysfunction, and obesity). The xenobiotic cleansing function of the liver and kidneys becomes less effective with increasing age due to a reduction in renal blood flow and glomerular filtration, rather than to a significant reduction in biotransformation capacity [37,40].

4.3. Sex and Hormonal Status

Some chemicals may be more toxic to one sex than to the other [41]. Also, variations in response to certain chemicals that are related to physiological differences between the sexes can affect hormonal systems and functions. Biologically, the difference is largely, if not exclusively, related to gonadal hormone secretion. Biological differences between the sexes contribute to many diseases and sex disorders [42,43]. Because male and female might have specific pharmacokinetic and pharmacodynamic differences, sex could affect the response to chemicals [44].
Previous studies have reported Hg accumulation in terms of the sex of the animal in cattle, studies of other species have shown higher levels of Hg accumulation in females than males [36]. For example, studies of deer and calves have shown higher levels of Hg accumulation in females [45]. It is of note that that study found no significant difference in Hg levels in the livers and kidneys between male and female deer. Experimental studies [46] have shown that the excretion and accumulation of Hg in animal organs are essentially influenced by the status of the reproductive hormones; however, as yet our understanding of the underlying mechanisms is incomplete.

5. Conclusions

High concentrations of Hg were found in the hair of cattle farmed in Bombana, both within and outside of ASGM areas. In the majority of cattle, the levels were much higher than the international regulatory limit for Hg in animals. The mean Hg concentration was higher in females than in males, but the difference was not statistically significant. Further, Hg concentration in cattle hair was positively correlated with the age of the cattle.
The mean Hg concentrations were highest in the hair of cattle farmed within ASGM areas, and the Hg concentrations in 80% of these cattle were potentially toxic. The possible cause of this contamination by mercury persistent in food chain. This contamination and its effects in cattle warrant further investigation.


The authors wish to thank the government of Bombana Regency, Indonesia for allowing us to conduct research, and its support with sampling. One author (B) wishes to thank the Indonesian Government for providing a Dikti Scholarship for graduate studies at Ehime University. This research (study) was supported by (and conducted as a part of) the Feasibility Study “Social Acceptance of Regional Innovation for Reducing High-Impact Environmental Pollution”, Research Institute for Humanity and Nature (RIHN). This work was supported by JSPS KAKENHI, Grant Number 16H02706 to Masayuki Sakakibara.

Author Contributions

All authors contributed extensively to the work presented in the paper. Basri as principal researcher conducted the analysis and wrote the manuscript, which was undertaken in association with his Ph.D. program. Masayuki Sakakibara, as Ph.D. supervisor, supervised the analyses and edited the manuscript. Koichiro Sera provided the PIXE measurement of hair samples. Idham Andri Kurniawan supported sample preparation and analyses.

Conflicts of Interest

The authors declare no conflict of interest.


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Figure 1. The location of the study (square line).
Figure 1. The location of the study (square line).
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Figure 2. The location of the samples site and distribution of Hg level.
Figure 2. The location of the samples site and distribution of Hg level.
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Figure 3. The normal probability plot of mean Hg both inside and outside the ASGM areas. (A) Sample values; (B) Logarithm of sample values.
Figure 3. The normal probability plot of mean Hg both inside and outside the ASGM areas. (A) Sample values; (B) Logarithm of sample values.
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Figure 4. The box plot of Hg concentration in cattle hair inside and outside the ASGM sites.
Figure 4. The box plot of Hg concentration in cattle hair inside and outside the ASGM sites.
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Figure 5. The plots of Hg concentration with respect to cattle age (A) inside the ASGM area, and (B) outside the ASGM area.
Figure 5. The plots of Hg concentration with respect to cattle age (A) inside the ASGM area, and (B) outside the ASGM area.
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Figure 6. The box plot of Hg concentration in cattle hair. (A) Hg concentration showed no significant difference with respect to animal sex. (B) The concentration of Hg in females was higher than in males in the two sampling sites.
Figure 6. The box plot of Hg concentration in cattle hair. (A) Hg concentration showed no significant difference with respect to animal sex. (B) The concentration of Hg in females was higher than in males in the two sampling sites.
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Table 1. Number, sex, and age of cattle, distribution by location and Hg concentration.
Table 1. Number, sex, and age of cattle, distribution by location and Hg concentration.
Animal DataSample LocationMann-Whitney U Test
Inside of ASGM Site (n = 34)Outside of ASGM Site (n = 29)
Hg levels (μg/g) and sample locationMean ± SD11.44 ± 9.522.89 ± 2.45p (0.000) < 0.05 *
Age (years) and sample locationMean ± SD6.00 ± 2.904.00 ± 3.07p (0.003) < 0.05 *
Hg levels (μg/g) sex and sample locationMale (n = 21)Mean ± SD10.17 ± 7.132.41 ± 2.40p (0.037) < 0.05 *
Female (n = 42)Mean ± SD11.98 ± 10.453.19 ± 2.51p (0.084) > 0.05 **
* Significant at p < 0.05; ** Non-significant at p > 0.05.

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Basri; Sakakibara, M.; Sera, K.; Kurniawan, I.A. Mercury Contamination of Cattle in Artisanal and Small-Scale Gold Mining in Bombana, Southeast Sulawesi, Indonesia. Geosciences 2017, 7, 133.

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Basri, Sakakibara M, Sera K, Kurniawan IA. Mercury Contamination of Cattle in Artisanal and Small-Scale Gold Mining in Bombana, Southeast Sulawesi, Indonesia. Geosciences. 2017; 7(4):133.

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Basri, Masayuki Sakakibara, Koichiro Sera, and Idham Andri Kurniawan. 2017. "Mercury Contamination of Cattle in Artisanal and Small-Scale Gold Mining in Bombana, Southeast Sulawesi, Indonesia" Geosciences 7, no. 4: 133.

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