Mercury Contamination in Riverine Sediments and Fish ... - MDPI

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Environmental Research and Public Health Article

Mercury Contamination in Riverine Sediments and Fish Associated with Artisanal and Small-Scale Gold Mining in Madre de Dios, Peru Gerardo Martinez 1, *, Stephen A. McCord 1 ID , Charles T. Driscoll 2 ID , Svetoslava Todorova 2 , Steven Wu 3 , Julio F. Araújo 4,5 , Claudia M. Vega 4,5 and Luis E. Fernandez 4,5 1 2 3 4 5

*

Department of Civil and Environmental Engineering, University of California, Davis, CA 95616, USA; [email protected] Department of Civil and Environmental Engineering, Syracuse University College of Engineering and Computer Science, Syracuse, NY 13244, USA; [email protected] (C.T.D.); [email protected] (S.T.) BioConsortia Inc., Davis, CA 95616, USA; [email protected] Centro de Innovación Científica Amazónica (CINCIA), Puerto Maldonado, Madre de Dios 17000, Peru; [email protected] (J.F.A.); [email protected] (C.M.V.); [email protected] (L.E.F.) Center for Energy, Environmental and Sustainability (CEES), Wake Forest University, Winston-Salem, NC 27109, USA Correspondence: [email protected]; Tel.: +1-310-910-2467

Received: 8 June 2018; Accepted: 23 July 2018; Published: 26 July 2018

Abstract: Artisanal and small-scale gold mining (ASGM) in Madre de Dios, Peru, continues to expand rapidly, raising concerns about increases in loading of mercury (Hg) to the environment. We measured physicochemical parameters in water and sampled and analyzed sediments and fish from multiple sites along one ASGM-impacted river and two unimpacted rivers in the region to examine whether Hg concentrations were elevated and possibly related to ASGM activity. We also analyzed the 308 fish samples, representing 36 species, for stable isotopes (δ15 N and δ13 C) to estimate their trophic position. Trophic position was positively correlated with the log-transformed Hg concentrations in fish among all sites. There was a lack of relationship between Hg concentrations in fish and either Hg concentrations in sediments or ASGM activity among sites, suggesting that fish Hg concentrations alone is not an ideal bioindicator of site-specific Hg contamination in the region. Fish Hg concentrations were not elevated in the ASGM-impacted river relative to the other two rivers; however, sediment Hg concentrations were highest in the ASGM-impacted river. Degraded habitat conditions and commensurate shifts in fish species and ecological processes may influence Hg bioaccumulation in the ASGM-impacted river. More research is needed on food web dynamics in the region to elucidate any effects caused by ASGM, especially through feeding relationships and food sources. Keywords: mercury; fish; sediment; artisanal and small-scale gold mining; Madre de Dios; Peruvian Amazon

1. Introduction Mercury (Hg) is a global pollutant that can affect both human and ecosystem health. It is a naturally-occurring element, but concentrations have been enriched due to mobilization by humans for thousands of years into the atmosphere, as well as aquatic and terrestrial ecosystems [1,2]. Over the past century, Hg emissions have increased due to increased industrialization associated with fossil fuel combustion, mining, and industrial products and processes [2,3].

Int. J. Environ. Res. Public Health 2018, 15, 1584; doi:10.3390/ijerph15081584

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Int. J. Environ. Res. Public Health 2018, 15, 1584

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Artisanal and small-scale gold mining (ASGM) currently accounts for an estimated 37% of global Hg emissions into the atmosphere [4,5]. Mercury-laden waste is also directly discharged into water bodies after gold refining processes. Mercury exposure can threaten wildlife and human health through the consumption of Hg-contaminated fish [6–8]. Thus, remote regions and communities near gold mining activities, such as the Amazonian region of Madre de Dios (MDD) in Peru, are highly susceptible to Hg contamination [9,10]. Peru is Latin America’s top gold producer, and currently the sixth largest gold producer globally, processing approximately 150 Mg in 2017 [11–13]. ASGM has been occurring in MDD for over 40 years [14]. From 1999 to 2012, land conversion for gold mining in MDD increased 400%, with approximately 50,000 ha of forest removed by 2012 [15]. From 2012 to 2016, another 20,000 ha was deforested due to gold mining in MDD [16]. Asner et al. [15,16] indicate that coinciding with the rapid expansion of mining zones there is also a marked increase in the number of miners. It is estimated that there are over 60,000 miners working in this region [17,18]. Peru signed the United Nations’ Minamata Convention in October 2013 and ratified it in January 2016. The Minamata Convention is a global treaty to limit Hg emissions and releases to the environment and protect human and environmental health from adverse effects of Hg. Despite this international management effort, extrajudicial gold mining continues to expand in Peru. ASG miners mix liquid elemental Hg with river sediments or soils to capture and amalgamate fine alluvial gold particles. The gold-mercury amalgam is heated in an open flame to volatilize the Hg and extract the gold [19,20]. A similar practice of adding liquid Hg to mined sediment slurries was practiced in California during the ‘Gold Rush’ (latter half of 1800s), leaving a legacy of Hg contamination that continues to plague the environment [21]. The toxicity and exposure of Hg is closely linked to the formation of methylmercury (MeHg). Ionic Hg can be converted by bacteria and archaea in anaerobic waters and sediments into the bioaccumulative and highly toxic form MeHg. Fish concentrate both ionic Hg and MeHg through consumption of water and aquatic organisms. However, the half-life of MeHg in fish is approximately two years, compared to almost three months for ionic Hg [22]. This slow loss, combined with continuous exposure, results in substantial MeHg accumulation along the food chain. Dietary consumption of fish is the primary pathway of human and wildlife exposure to MeHg, a potent neurotoxin that can significantly impair human health [2]. More than 95% of the total Hg present in fish muscle tissue is MeHg [23]. Consequently, larger predatory fish generally have the highest MeHg concentrations [24]. Approximately 75% of total fish captures in the Peruvian Amazon are from subsistence fisheries; therefore, MeHg exposure in regions such as MDD is an important concern for riverine and indigenous populations that subsist on local fish [25]. Mercury concentrations are difficult to predict and track in aquatic ecosystems because of their complex interactions with multiple physical and biogeochemical factors that drive its transport, transformations and fate [26]. Diringer et al. [27] found higher Hg concentrations in fish (Hgfish ) and sediment (Hgsed ) at sites downstream from ASGM activities in comparison to upstream sites along the Madre de Dios River. Previous research in the study area have reported elevated Hg concentrations in human hair and in commercial fish species in locations with ASGM activities as well as in locations without ASGM activities [19,27–32]. Fish sampling in these rivers is difficult because waters tend to be uninhabitable by fish due to high turbidity from very high suspended solids loads [33]. In this study, we evaluated Hgsed and Hgfish in a river where mining activities were occurring upstream and compared these values to those from two proximate rivers without mining to characterize the level and extent of Hg contamination associated with ASGM. The objective of our study was to evaluate if proximity to ASGM is enriching Hgsed and Hgfish in the rivers. We also wanted to address two subsidiary questions: (1) How do Hgfish vary by species, trophic position, and size? and (2) Do Hgfish vary seasonally?

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2. Materials and Methods 2. Materials and Methods 2.1.2.1. Site Description Site Description MDD in the theAmazon Amazon rainforest in southeast Peru bordering Brazil andPuerto Bolivia. MDDisislocated located in rainforest in southeast Peru bordering Brazil and Bolivia. ◦ S, 69.1963◦ W) is the capital city of MDD. Madre de Dios, which directly Puerto Maldonado (12.5909 Maldonado (12.5909° S, 69.1963° W) is the capital city of MDD. Madre de Dios, which directly translates asas “Mother capitalof ofPeru”. Peru”.ItItisisconsidered considered one translates “MotherofofGod,” God,”isisknown knownas as the the “biodiversity “biodiversity capital one of of most biodiverseecosystems ecosystemsininthe theworld world and and has has been been prioritized [34,35]. The thethe most biodiverse prioritizedfor forconservation conservation [34,35]. The construction of Interoceanic the Interoceanic Highway, a roadway which approximately spans approximately km construction of the Highway, a roadway which spans 2600 km 2600 connecting connecting Peru line), (Figure 1, to dashed line), has led toindustrialization, increased urbanization, Brazil and PeruBrazil (Figureand 1, dashed has led increased urbanization, and natural industrialization, and natural resource extraction, all of which have degraded the environment resource extraction, all of which have degraded the environment [36]. In particular, 70,000 ha of[36]. virgin In particular, hafor of virgin forest have been cleared for gold mining and an estimated 40–45 Mg forest have been70,000 cleared gold mining and an estimated 40–45 Mg of elemental Hg are used annually of elemental Hg are used annually by miners to amalgamate gold flakes in excavated soil [14,16]. by miners to amalgamate gold flakes in excavated soil [14,16]. This study wasconducted conductedon onthree three rivers rivers in in MDD. MDD. The rivers areare This study was The Tambopata Tambopataand andMalinowski Malinowski rivers located southwest of the district capital, in the Tambopata National Reserve. Tambopata River located southwest of the district capital, in the Tambopata National Reserve. Tambopata River receives receives inputs from the mining-impacted Malinowski River (Figure 1, circled in red). We sampled inputs from the mining-impacted Malinowski River (Figure 1, circled in red). We sampled Tambopata Tambopata River upstream from its confluence with Malinowski River (Figure 1, circled in green). River upstream from its confluence with Malinowski River (Figure 1, circled in green). Studies show Studies show that forest loss from ASGM on the upper Malinowski River has largely increased in the that forest loss from ASGM on the upper Malinowski River has largely increased in the last decade [16]. last decade [16]. The Heath River (circled in blue, Figure 1) is located southeast of the district capital The Heath River (circled in blue, Figure 1) is located southeast of the district capital in an undisturbed in an undisturbed watershed within the Bahuaja Sonene National Park. This river forms the border watershed the Bahuaja Sonene Park. This river forms in the border between and between within Peru and Bolivia. There have National been no known mining activities the national park upPeru to the Bolivia. There have been no known mining activities in the national park up to the time of this study. time of this study.

Figure 1. Map of the study region. Fish sampling for each season was conducted in the circled reaches Figure 1. Map of the study region. Fish sampling for each season was conducted in the circled reaches for each river Tambopata River (green), Malinowski River (red), and Heath River (blue). Circles for each river Tambopata River (green), Malinowski River (red), and Heath River (blue). Circles indicate indicate sediment sample sites. The Interoceanic Highway is denoted with a dashed line. sediment sample sites. The Interoceanic Highway is denoted with a dashed line.

2.2. Sampling and Sample Processing Procedures

2.2. Sampling and Sample Processing Procedures

Wet season sampling was conducted in January–February 2017. Dry season sampling was Wet season sampling wasWet conducted in January–February 2017. Dry season sampling was conducted in August 2017. season sampling was challenging because fish dispersed into conducted in August 2017. Wet season sampling was challenging because fish dispersed into floodplains and debris hindered boat travel. Nevertheless, fish and sediment samples were collected

floodplains and debris hindered boat travel. Nevertheless, fish and sediment samples were collected


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in both seasons. Sediment samples were collected using an Ekman dredge in quiescent pools with predominantly fine sediments. To complement river sediments, shoreline samples were also collected from recently submerged areas (following storm peaks) using a 2-cm deep, 10-cm wide stainless-steel scoop. All sediment collection equipment was rinsed thoroughly with deionized water between sample collections. Fish samples were collected using drag nets, gill nets, and hook and line based on conditions at each site. Lengths (L, mm) and wet weight (WW, kg) were measured for each individual fish in the field. During wet season sampling, strong currents proved difficult for certain fishing techniques, particularly drag nets. During dry season sampling, with low-flow and low-water levels, all fishing techniques were viable. The majority of fish species caught were commercially important species, easily identified in the field. For less common fish species, identification was based on feeding habits and sampling location according to taxonomy keys [37,38]. For fish longer than 10 cm, a scalpel was used to remove the skin and scales from just below the dorsal fin of the left side of each fish. An 8-mm Acuderm biopsy punch (Acuderm Inc, Ft. Lauderdale, FL, USA) was then used to extract a small, subcutaneous “plug” of fish tissue for analysis. Several studies have shown that there is little variation between traditional, fish filet samples and fish plug samples [39–42]. For fish less than 10-cm long, a scalpel was used to remove the skin and a standard fillet sample was taken from the left side of the fish. All research protocols involving fish subjects were approved by Servicio Nacional de Áreas Naturales Protegidas por el Estado (Resolución Directoral N◦ 010-2017-SERNANP-DGANP). We visited a total of 25 fish sampling sites: nine on Tambopata River, six on Malinowski River, and ten on Heath River (Supplementary Materials, Table S1). All fish sampling sites for Tambopata and Malinowski rivers were located upstream from their confluence. A total of 308 fish samples were collected during both seasons. During each cruise, fish and sediment samples were preserved on wet ice. Upon arrival in Puerto Maldonado, all samples were immediately stored at −20 ◦ C. Samples were then transported with ice in a Cr¯edo ProMed® cooler (Pelican BioThermal, Plymouth, MN, USA) to Syracuse University in Syracuse, NY for analyses. Physicochemical water quality parameters (pH, temperature, dissolved oxygen, and nitrate) were measured in-situ at each site using a YSI Sonde (YSI Inc., Yellow Springs, OH, USA), Hanna pH Tester (Hanna Instruments, Woonsocket, RI, USA), and a LaMotte Dissolved Oxygen Test Kit (LaMotte Company, Chestertown, MD, USA). Turbidity was measured using a Hach 2100Q Portable Turbidimeter (Hach Company, Loveland, CO, USA). 2.3. Chemical Analyses Upon arrival at Syracuse University, all samples were freeze-dried dried at −80 ◦ C and 0.080 mBar using FreeZone: Type 6 plus freeze drier by Labconco (Labconco Corp., Kansas City, MO, USA). After freeze-drying, fish samples were homogenized and analyzed for total Hg using a Milestone Direct Mercury Analyzer (DMA-80, Milestone Inc., Shelton CT, USA) following US EPA Method 7473 [43]. Sediment samples were sieved and the fraction of particle sizes 5 individuals were collected. we attempted to normalize fish to median lengths for species for which >5 individuals were collected. However, Hg fish were not strongly correlated with length. Therefore, we present unadjusted Hg fish. However, Hgfish were not strongly correlated with length. Therefore, we present unadjusted Hgfish . Hgfish ranged from 0.01 mg/kg to 1.50 mg/kg (median 0.14 mg/kg). The highest Hg fish was found in a Hg fish ranged from 0.01 mg/kg to 1.50 mg/kg (median 0.14 mg/kg). The highest Hgfish was found in apiscivorous piscivorouspaña pañaSerrasalmus Serrasalmusspp. spp.(1.50 (1.50mg/kg) mg/kg)sampled sampledininthe theASGM-impacted ASGM-impactedMalinowski MalinowskiRiver. River.


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The fish was only 79 mm long. The longest fish sampled was 980 mm, a piscivorous puma zungaro Pseudoplatystoma tigrinum (0.82 mg/kg) caught in Heath River. 3.3.2. Wet vs. Dry Season The mean Hgfish in Malinowski River was significantly higher in the dry season (0.28 ± 0.24 mg/kg) than in the wet season (0.18 ± 0.15 mg/kg, p = 0.028) (Table 2). However, for Tambopata and Heath rivers mean Hgfish were similar in the wet (Tambopata: 0.23 ± 0.23 mg/kg; Heath; 0.20 ± 0.22 mg/kg) and dry seasons (Tambopata: 0.22 ± 0.27 mg/kg, p = 0.508; Heath: 0.19 ± 0.27 mg/kg, p = 0.072). ANOVA among rivers and seasons showed there was no significant difference between seasons (p = 0.33). Therefore, subsequent comparisons are based on data combined for both seasons. Table 2. Mean fish Hg concentrations (±standard deviation) for each season. River

Season

Mean Hgfish (mg/kg)

Tambopata

Wet Dry

0.23 ± 0.23 0.22 ± 0.27

Wet

0.18 ± 0.15

Malinowski Insects 2017, 8, xInsects FOR PEER 2017, Dry 8, REVIEW x FOR PEER REVIEW 0.28 ± 0.24 Insects 2017, 8, x FOR PEER REVIEW Wet

Insects 0.20 ±2017, 0.22 8, x FOR PEER REVIEW Dry 0.19 ± 0.27 Table 1. Number Table of1.oceanic Number seaofskaters, oceanicHalobates, sea skaters, collected Halobates, at locations collectedinatthe locations tropicalinPacific the tropical OceanP total1.number ofof individuals numbersea ofcollected; individuals collected; Halobates H.g.: germanus, Halobates H.m.: germanus, H. H.m.: Stat: H.station micans;collected number; Stat: stati Table Numbertotal oceanic skaters, H.g.: Halobates, Table 1.collected Number at oflocations oceanic sea inmicans; the skaters, tropical Halobates, Pacific Ocean onW a 3.3.3. Fish Isotopic Values (δ15 N and δ13 C) larvae; A:Halobates, number larvae; of A: adults, number E: locations number of adults, exuviae; number EG: of number exuviae; of EG: eggs number of eggs (on such substrates asgermanus polystyr su total number of individuals collected; H.g.:of total Halobates number germanus, ofPacific individuals H.m.: H. collected; micans; Stat: H.g.: station Halobates number; WT: Table 1. Number of oceanic sea skaters, collected at inE: the tropical Ocean on(on 7–8substrates December2016,during the 15 min; Sa: salinity 15of min; (‰); Sa:(9.4 S: salinity (‰); area S:micans; swept surface by area the neuston sweptof by net the expressed neuston net as the expressed value ofasthe theflow-m value larvae; A:H.g.: number adults, E:surface number offor exuviae; larvae; A: EG: number number of adults, eggs (on E: substrates of exuviae; such as polystyren EG: numbe The δof15individuals N values ranged from 3.9 to 12.4 ± 1.5 )H. the entire dataset. Mean δ15number N values total number collected; Halobates germanus, H.m.: Stat: station number; WT: water temperature (°C); AT: a Insects 2017, 8, x FOR Insects PEER 2017, REVIEW 8, x FOR PEER REVIEW (m/s); W: weather; (m/s); TD: W: weather; time of day; TD: CS: time current of day; speed CS: current (m/s); CD: speed current (m/s); direction; CD: current F: female; direction; M: F: male fem 15number min; (‰); surface of area swept 15 min; by the Sa:(9.6 neuston salinity net (‰); expressed S: surface asform); area the value swept by the theflow-mete neuston larvae; number adults, E: ofsalinity exuviae; EG: number (on substrates such as polystyrene Date:of sampling date; wereA:lowest inofTambopata RiverSa:(8.6 ± 1.4 ), S: followed byeggs Heath River ± 1.4 ) and Malinowski Insects 2017, 8, x FOR PEER REVIEW 2 area. (m/s); W: weather; TD: of day; CS: (m/s); W: weather; (m/s); TD:flow-meter current time ofdirection; day; CS:mcurrent F:of female; M: male. (m/s); C 15 River min; Sa: salinity surface area swept area. by the time neuston net expressed asspeed the value ofCD: the × 1.3 thespeed width of theN (9.8 ± 1.4(‰); ). S: Two-way ANOVA showed there was nocurrent significant difference between seasons

Insects 2017, 8, x FOR PEER REVIEW


Heath


area. (m/s); weather; TD: time CS: current speed Table (m/s); CD: the current direction; F:A