This study examined the transport and accumulation of mercury in the Madre de Dios River watershed in Peru resulting from artisanal and small-scale gold mining (ASGM) activity. Samples of river sediment, suspended solids, and fish were collected at 62 sites along a 560 km stretch of the river near 17 communities. Mercury concentrations in these samples increased with proximity to known ASGM areas, demonstrating a gradient of contamination moving downstream. Over one-third of predatory fish species sampled exceeded international health standards for mercury, representing a risk of dietary mercury exposure for local communities hundreds of kilometers from mining sites. This is the first systematic study to characterize mercury pollution and human health risks in this region where ASGM is a major

1. See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/269775984
River Transport of Mercury from Artisanal and
Small-Scale Gold Mining and Risks for Dietary
Mercury Exposure in Madre de Dios, Peru
Article in Environmental Sciences: Processes and Impacts · December 2014
Impact Factor: 2.17 · DOI: 10.1039/C4EM00567H
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2. River transport of mercury from artisanal and
small-scale gold mining and risks for dietary
mercury exposure in Madre de Dios, Peru†
Sarah E. Diringer,a
Beth J. Feingold,‡bc
Ernesto J. Ortiz,c
John A. Gallis,cd
Julio M. Ara´ujo-Flores,e
Axel Berky,b
William K. Y. Pan*bc
and Heileen Hsu-Kim*a
Artisanal and small-scale gold mining (ASGM) is a major contributor to deforestation and the largest
anthropogenic source of atmospheric mercury worldwide. Despite significant information on the direct
health impacts of mercury to ASGM miners, the impact of mercury contamination on downstream
communities has not been well characterized, particularly in Peru's Madre de Dios region. In this area,
ASGM has increased significantly since 2000 and has led to substantial political and social controversy.
This research examined the spatial distribution and transport of mercury through the Madre de Dios
River with distance from ASGM activity. This study also characterized risks for dietary mercury exposure
to local residents who depend on fish from the river. River sediment, suspended solids from the water
column, and fish samples were collected in 2013 at 62 sites near 17 communities over a 560 km stretch
of the Madre de Dios River and its major tributaries. In areas downstream of known ASGM activity,
mercury concentrations in sediment, suspended solids, and fish within the Madre de Dios River were
elevated relative to locations upstream of mining. Fish tissue mercury concentrations were observed at
levels representing a public health threat, with greater than one-third of carnivorous fish exceeding the
international health standard of 0.5 mg kgÀ1
. This study demonstrates that communities located
hundreds of kilometers downstream of ASGM activity, including children and indigenous populations
who may not be involved in mining, are at risk of dietary mercury exposure that exceed acceptable body
burdens. This report represents the first systematic study of the region to aid policy decision-making
related to ASGM activities in Peru.
Environmental impact
Artisanal and small-scale gold mining (ASGM) is the largest anthropogenic source of mercury to the atmosphere. While the impacts of ASGM to the health of
miners have been studied in great detail, the implications for water quality in local watersheds have not. This study is the rst to describe the extent of mercury
release in the Madre de Dios watershed, a biodiversity hotspot within the Peruvian Amazon where ASGM activity is prevalent. The results demonstrate a gradient
of increasing mercury contamination in the river downstream of mining areas and signicant risk of dietary mercury exposure for community members who eat
sh hundreds of kilometers from the mining activity.
Introduction
Artisanal and small-scale gold mining (ASGM) is a largely
unregulated sector of the global economy in more than 70
countries and is rising at a dramatic rate.1,2
During the mining
process, elemental mercury Hg(0) is added to large quantities of
sediment and soils that have been exhumed from riverbanks
and forested areas. Mercury forms a strong bond with gold to
separate it from the river sediments or solids. The gold–mercury
amalgam is then heated in the eld and in gold shops to
separate the metals. Miners involved in amalgam burning are
exposed to extremely high levels of Hg(0) and have greater
incidence of neurological disorders and kidney dysfunction, a
common side effect of Hg(0) inhalation.3
Along with
a
Department of Civil and Environmental Engineering, Pratt School of Engineering,
Duke University, 121 Hudson Hall, Box 90287, Durham, NC 27710, USA. E-mail:
hsukim@duke.edu; Tel: +1(919)-660-5109
b
Nicholas School of the Environment, Duke University, 450 Research Dr, Durham, NC
27710, USA. E-mail: william.pan@duke.edu; Tel: +1(919)-684-4108
c
Duke Global Health Institute, Duke University, 310 Trent Dr, Durham, NC 27710, USA
d
Department of Biostatistics and Bioinformatics, Duke University Medical Center,
DUMC Box 2721, Durham, NC 27710, USA
e
Department of Environmental Biology and Public Health, University of Huelva,
Campus El Carmen 21071, Huelva, Spain
† Electronic supplementary information (ESI) available. See DOI:
10.1039/c4em00567h
‡ Current affiliation: Department of Environmental Health Sciences, School of
Public Health, University at Albany, George Education Center, Room 145, One
University Place, Rensselaer, NY 12144, USA.
Cite this: DOI: 10.1039/c4em00567h
Received 21st October 2014
Accepted 19th December 2014
DOI: 10.1039/c4em00567h
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3. contributing signicantly to deforestation, ASGM has surpassed
fossil fuel combustion as the largest anthropogenic source of
mercury (Hg) to the global atmosphere.2
Up to 60% of the Hg
used in ASGM is released directly to the environment and can
accumulate in sediment on site, in the atmosphere, and in
downstream rivers.4
In river sediments, anaerobic microorganisms methylate Hg
to produce monomethylmercury (MeHg), a highly neurotoxic
form of Hg that biomagnies in aquatic food webs.5
In humans,
excess MeHg intake through sh consumption can decrease
cognitive and kidney function. Moreover, MeHg is capable of
crossing the placental barrier to affect fetuses in pregnant
women, leading to impaired neurodevelopment, cognitive
function, and motor skills. Fish is an important food source for
both nutrition and culture in communities throughout the
world and is an especially important source of nutrients for
children.6–8
People who are not involved directly in ASGM but
live near mining sites oen have their greatest Hg exposure
from sh consumption.9,10
Thus, the bioaccumulation of MeHg
in sh poses signicant human health risks for these commu-
nities, especially for children and women of childbearing age.
The Madre de Dios (MDD) region of Peru is located in the
headwaters of the tropical Amazon. It is one of the world's most
biodiverse ecosystems and a prioritized biodiversity hotspot for
conservation.11
ASGM has occurred in the MDD region since the
1970's. However, activity has grown immensely since the early
2000's, corresponding with the signicant increases in the
international gold price.1
The extent of land use for gold mining
in the MDD region increased by 400% between 1999 and 2012.12
With this increase in ASGM activity, rapid deforestation has
been recorded, including nearly 2000 ha per year of newly
deforested area between 2006 and 2009.1
ASGM provides an
important source of income in the MDD region. Unconrmed
reports have estimated that ASGM employs between 10 000 and
30 000 active miners in the MDD region and makes up nearly
50% of the local economy.9,13,14
While Hg use for ASGM is
widespread in the region, the release of this metal to the
surrounding watershed and the implications for human expo-
sure have not been studied in a systematic manner. Neverthe-
less, the Peruvian government has recently begun to enforce
regulatory requirements for ASGM with military action and
embargos on gasoline, resulting in riots and signicant social
unrest.15,16
With these economic and social implications at
stake, it is imperative that the environmental and health
impacts of Hg from ASGM are quantied.
The specic objectives of this study were to: (1) examine the
distribution of Hg in the MDD River environment at points
upstream and downstream of ASGM activities; (2) examine
transport of Hg from concentrated areas of mining through
direct release and runoff; and (3) evaluate potential risks of
dietary Hg exposure via sh for communities along the river.
Study region
The study region included the portion of the MDD River starting
at Atalaya (located at km 1) to Puerto Pardo (located at km 560
downstream) at the Peru-Bolivia border (Fig. 1). For analysis and
discussion purposes, the MDD River was divided into three
sections to determine the inuence of ASGM on Hg in the river.
Section 1 (km 1 to 180) represents the upstream area with little
or no active ASGM activity. Beginning near km 180, ASGM
occurred with the greatest density along the MDD River up to
km 400.12
Moreover, the most concentrated areas of mining
activity have been focused along two major tributaries that feed
into the MDD River: the Colorado and Inambari Rivers with
outlets at km 225 and 356 respectively.1,12
These areas (known as
Huepetuhe, Guacamayo, and Delta-1) represent approximately
50% of the total gold mining in the region.1,12
Section 3 (km 401
to km 560) contains fewer active ASGM areas and the large
population center of Puerto Maldonado where a large number
of gold shops are located. Additional samples were collected at
Lago Valencia, an oxbow lake in Section 3 at km 545 that has
seasonal sediment exchange during the wet season (roughly
November–March) and limited exchange during the dry season
(roughly April–October). Fishing is common in Lago Valencia,
and most of the sh caught within the lake are sold in areas
between Puerto Maldonado and Puerto Pardo.
Materials and methods
Field methods
Two sampling events were performed in 2013: once during the
wet season (March–April) and once during the dry season (June–
July). Sediment and whole water samples were collected at 62
sites along a 560 km reach of the MDD River from Atalaya (km 1)
through Puerto Pardo (km 560 downstream) at the Peru-Bolivia
Border. Sites on the MDD River included locations within 3 km
upstream and 3 km downstream of conuences with major
tributaries (Manu, Colorado, Inambari, and Tambopata Rivers).
Additional samples were collected on each of the major
tributaries approximately 1 km upstream of the conuence with
the MDD River. At each site, a water quality data sonde
(Professional Plus Pro, YSI, Incorporated, Yellowsprings, Ohio)
was deployed in the water at mid-channel for quantication of
pH, dissolved oxygen, conductivity, and temperature.
Surface water samples were collected in duplicate or tripli-
cate at mid-channel and <0.5 m depth using 1 L pre-cleaned
polyethylene containers (VWR). Whole water samples were
ltered in the eld using pre-weighed 0.22 mm glass ber lters
(Whatman QM-A grade) placed on a polyethylene vacuum
ltration apparatus for total suspended solids (TSS) and total
suspended particulate Hg (HgP) concentrations. Filters for TSS
were placed in plastic bags for storage. Filters for HgP were
placed in glass vials with uoropolymer-lined screw caps (pre-
cleaned vials for trace mercury analysis from Brooks Rand).
Sediment samples were obtained in triplicate at locations
within 2 m of the bank edge on both sides of the river. Sediment
from the top 5 cm were scooped by gloved hand and placed into
trace metal-cleaned polyethylene containers (VWR). All samples
were placed on dry ice and frozen at À20
C in the eld using
Credo Cube Series 20M (Minnesota Thermal Science, Plymouth,
MN). Samples were then shipped and stored at À20
C upon
return to the laboratory at Duke University.
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4. Analysis of Hg concentration in ltered water samples,
which typically includes dissolved and colloidal Hg phases, was
not performed due to the lack of immediate access to trace-
metal clean facilities to preserve these samples within 2–3 days
of collection. Mercury in surface waters, however, tends to be
predominantly associated with large particles (0.22 mm).17–19
Thus, with the study's aim to assess the extent of mercury
contamination over the entire reach of the river, we focused
research efforts on the quantication of suspended particulate
Hg concentration (HgP) in the river water column.
Surface water velocity was measured in the MDD River and
the four tributaries during the June/July 2013 sampling event.
For these measurements, a buoyant surface oat was released
from the boat and allowed to reach steady speed in the river.
Travel time of the oat for a dened distance was observed from
shore and recorded as the surface water velocity. Cross-sectional
area at each site was estimated using river width and depth at
three equally spaced points across a transect of the river. River
discharge rates were calculated for each location by multiplying
the cross-sectional area with the surface water velocity.
Whole sh were obtained by local shermen at 37 of the
sediment/water sampling sites along the MDD River using
traditional shing techniques, including cast net, overnight
netting, and hook-and-line. A total of 200 sh were collected
during both seasons, including 123 carnivorous sh, 74 non-
carnivorous sh, and 3 unknown. Fish were weighed,
measured, and identied in the eld, with identication
conrmed through photos. Carnivorous sh included piscivo-
rous, insectivorous, and omnivorous sh species. Fish scales
were removed in the eld and skin was removed upon return to
the laboratory at Duke University. Fish muscle-tissue samples
were obtained in triplicate from the anterior portion of each sh
above the lateral line. Samples were frozen at À20
C in the eld
and then shipped and stored at À20
C upon return to the
laboratory at Duke University.
Chemical analyses
Total Hg concentration in sediments and sh muscle tissue
were determined by direct thermal decomposition, amalgam-
ation, and atomic absorption spectrometry (Milestone DMA-
80).20
Total Hg was quantied as a proxy for MeHg in sh tissue
since generally 80% of Hg in sh tissue is in the form of
MeHg.21
Analysis of standard reference materials for Hg in
sediment (NIST 2709a) and sh (DORM-3 and DORM-4) by this
method resulted in recoveries of 98% Æ 5% SD (n ¼ 52), 103% Æ
4% SD (n ¼ 28), and 101% Æ 5% SD (n ¼ 33), respectively.
Fig. 1 Environmental and human health study sites in the Madre de Dios (MDD) watershed in Peru. Communities (red circles) on the MDD River
near sampling sites for sediment, water, and fish. Known regions of mining layers are courtesy of the Asociaci´on para la Conservaci´on de la
Cuenca Amaz´onica (ACCA) and denoted in pink; concentrated areas of mining include the Huepetuhe/Delta-1 mining area (red) and the
Guacamayo mining area (orange).
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5. Methylmercury concentration in sediments was determined
by dichloromethane extraction, aqueous phase ethylation,
purge-trap on Tenax resin and gas chromatographic separation,
and inductively coupled plasma mass spectrometry (Tekran
2600, Agilent 7700).22
A stable MeHg isotope (Me201
Hg) was
added to each sample as an internal standard prior to the
extraction step. MeHg concentrations were corrected for each
individual sample based on the recovery of its respective stable
isotope spike. Extractions that achieved stable isotope recov-
eries between 75% and 125% were accepted in the data set. The
average recovery was 87%.
Filters analyzed for TSS were dried at 104
C for 4 h and
weighed to determine total suspended particulate mass. Filters
for HgP determination were dissolved in 3 : 7 sulfuric acid–
nitric acid and heated at 60
C for 16 h. The extracts were
preserved with 1% v/v bromine monochloride, stored at room
temperature for at least 12 h, and analyzed by stannous chloride
(SnCl2) reduction, gold amalgamation, and cold vapor atomic
uorescence spectroscopy (MERX-T, Brooks Rand).17,22
Trace
metal grade acids (VWR) were used for digestion reagents, and
method blanks were performed to ensure that background Hg
concentration was below instrument detection limits. The total
Hg quantied on each 0.22 mm glass-ber lter was divided by
the volume of water passed through the lter to yield the
particulate mercury concentration (HgP, ng LÀ1
). The concen-
tration of Hg per mass of suspended solid (HgSS, ng gÀ1
) was
calculated from the HgP value divided by the TSS concentration
(mg LÀ1
).
Statistical methods
Descriptive statistics stratied by season were produced for the
concentrations mentioned above using means, standard devi-
ations (SD), and 95% condence intervals (C.I.) (Table 1).
Comparisons of river sections in regards to total Hg in
sediment, MeHg in sediment, Hgp and TSS were performed with
ordinary least squares (OLS) regression analysis of the raw
averages of duplicate or triplicate eld samples at each site.
Sites with only a single measurement were excluded from the
analysis. Total Hg in sediment, MeHg in sediment, Hgp and TSS
concentrations in the three river sections were estimated from
the OLS models. Linear splines were created for each of the
three sections in order to compare spatial changes in Hg
concentrations between each section (Table S1†). Each section
was also compared using a simple categorical variable for
stream section (Tables S2 and S3†). Suspended particle (TSS and
HgP) models were adjusted for season.
Fish tissue Hg concentrations were also compared between
sections for carnivorous and non-carnivorous sh (Table 2).
Correlations between sh parameters (e.g., Hg concentration,
sh diet, sh length, sh weight, and river section) were
examined using Pearson correlations (denoted PC). Statistical
signicance was dened as p 0.05. All statistical analyses were
performed using SAS version 9.4 (SAS Institute, Cary, NC).
Results and discussion
Mercury distribution in the Madre de Dios River
Total mercury concentrations in sediment increased with
distance downstream along the MDD River (Fig. 2, Tables 1 and
S3†). In locations upstream of known mining inuences (km 1
to 180; Section 1), Hg concentrations averaged 9.0 ng gÀ1
(95%
C.I. 1.5, 16.6). Total Hg concentrations in sediment in Section 2
near active mining (km 181 to 400) were signicantly greater
than in Section 1 by approximately 13.5 ng gÀ1
(95% C.I. 4.4,
22.6; p ¼ 0.004). Sediment concentrations continued to increase
signicantly in Section 3, downstream of the dense mining
activity with an average of 21.9 ng gÀ1
(95% C.I. 11.5, 32.4;
p 0.001) greater sediment Hg in Section 3 than in Section 1. The
greatest observed Hg concentration in sediment (up to 95.3 ng gÀ1
)
was measured in Section 3 at Palma Real (km 538) (Fig. 2a). The
increase in the average concentration from Section 2 to Section
3 was nearly signicant (p ¼ 0.064) and indicates continued
input of mercury to Section 3. Further, sediment Hg concen-
trations within Inambari River, which drains the Huepetuhe
and Guacamayo mining areas, were twice as high on average
compared to the MDD River upstream of the tributary (19.2 mg
kgÀ1
compared to 39.6 mg kgÀ1
). This suggests new inputs of Hg
and transport of contaminated sediments to areas downstream
of large mining areas. Sediment concentrations did not vary
signicantly between seasons (p ¼ 0.66), so the model was not
adjusted for season.
Table 1 Average concentrations of total mercury (HgT), methylmercury (MeHg), suspended particulate mercury (HgP), and Total Suspended
Solids (TSS) in each section with 95% confidence intervals based on ordinary least squares regression analysis
Total Hg
(mg kgÀ1
)
n ¼ 59
MeHg
(pg gÀ1
)
n ¼ 20
Suspended particulate Hg (HgP),
(ng LÀ1
) Total suspended solids (mg kgÀ1
)
Dry season,
season 2
Wet season,
season 1
Dry season,
season 2
Wet season,
season 1
River Section 1
(km 1 to 180)
9.0 (1.4, 16.6) 32.5 (À268.4, 333.4) 0.4 (À3.2, 3.9) 7.0 (3.5, 10.6) 124.8 (30.2, 29.5) 526.5 (437.3, 615.8)
River Section 2
(km 181 to 400)
22.6 (17.4, 27.7) 277.7 (159.7, 395.8) 10.4 (7.6, 13.1) 17.0 (14.2, 19.8) 215.0 (140.5, 290.3) 617.1 (545.8, 688.4)
River Section 3
(km 401 to 560)
31.0 (23.7, 38.3) 102.5 (À85.9, 292.8) 15.0 (11.6, 18.3) 21.6 (18.3, 25.0) 112.4 (21.7, 203.0) 514.1 (426.0, 602.1)
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6. The concentration of methylmercury (MeHg) in the sedi-
ments and the percent of the total Hg as MeHg (%MeHg)
increased with proximity to mining areas (Fig. 2b and c). At sites
in Section 2, proximal to the greatest density of active mining
activities, MeHg concentrations reached concentrations that
were more than ten times the maximum concentrations found
in Section 1 (670 pg gÀ1
compared to 43.8 pg gÀ1
; Fig. 2b). The
largest MeHg concentration (837 ng gÀ1
) for the entire study was
observed in the Inambari River. The average concentrations in
Section 2 were 254.8 pg gÀ1
(95% C.I. 22.8, 486.9; p ¼ 0.03) and
greater than in Section 1. The average MeHg concentration was
also greater in Section 2 than in Section 3, though not statisti-
cally signicant for alpha ¼ 0.05 (p ¼ 0.11; Table S3†). The
increase in MeHg from Section 1 to Sections 2 and 3 also cor-
responded with increased temperature and decreased dissolved
oxygen (Fig. S1†), which may indicate conditions suitable for
MeHg production. However, there were no apparent correla-
tions between sediment or water quality parameters that
directly impacted MeHg concentration or percent. Average Hg
and MeHg in sediment as well as condence intervals within
each river section can be found in Table S2.†
These results collectively indicate that portions of the MDD
River downstream of mining activity not only had signicantly
greater total Hg content in sediments, but also appeared to host
locations with large net methylation potential for mercury, as
indicated by the greater %MeHg values in downstream sites
relative to upstream sites. While MeHg generally represented a
small proportion of the total Hg in the MDD River sediments
(3% as MeHg), this type of Hg can biomagnify within the food
chain and is the major form of mercury in sh muscle
tissue.23–25
Areas with relatively greater %MeHg values may
signify regions of the river with high bioaccumulation potential.
Mercury and particle transport in the Madre de Dios River
In river systems, suspended particles play an important role in
Hg transport, as the predominant fraction of Hg is typically
associated with particulate matter in the water column.17–19
Total suspended solids (TSS) concentrations were generally
greater during the March–April wet season than in the June–July
dry season (p 0.01) (Fig. 3a). The large scatter in the data is
likely due to rain events, which were not removed from the data
series. During each sampling season, Section 2 contained the
greatest average TSS concentrations relative to the other
Table 2 Total Hg concentrations in fish muscle tissue (mg kgÀ1
) from the Madre de Dios River and the percentage of fish exceeding 0.5 mg kgÀ1
,
the World Health Organization (WHO) standard
Non-carnivorous sh Carnivorous/omnivorous sh
Location in Madre de Dios
River: communities affected
Average Hg conc. in mg kgÀ1
(95% C.I.)
% Exceeding WHO
threshold
Average Hg conc. in mg kgÀ1
(95% C.I.)
% Exceeding WHO
threshold
Section 1 (km 1 to 180):
Atalaya through Tambo
Blanquillo
0.08 (0.00, 0.17) 0% (0/13) 0.20 (0.01, 0.39) 6% (1/18)
Section 2 (km 181 to 400):
Tambo Blanquillo through
Laberinto
0.29 (0.24, 0.34) 12% (5/41) 0.77 (0.64, 0.90) 55% (26/47)
Section 3 (km 401 to 560):
Tres Islas to Puerto Pardoa
0.18 (0.11, 0.26) 9% (1/20) 0.34 (0.22, 0.45) 24% (14/58)
Lago Valencia (km 545) 0.14 (0.07, 0.21) 0% (0/9) 0.45 (0.20, 0.70) 50% (4/8)
a
Section 3 includes Lago Valencia (km 545).
Fig. 2 (a) Total mercury (Hg) concentrations and (b) methylmercury
(MeHg) concentrations (dry weight basis) in bottom river sediment of
the MDD River and major tributaries to the river; (c) the percentage of
the total Hg as MeHg in sediments. Each data point represents the
average of all samples at one field site collected during the wet season
(March–April) and dry season (June–July) of 2013. Error bars are
standard deviations of the average field sample (n ¼ 2–3).
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7. sections of the river for the same season. The average TSS in
Section 2 was 228 mg LÀ1
(95% C.I. 161, 295) during the dry
season and 642 mg LÀ1
(95% C.I. 574, 711) during the wet
season. TSS concentrations in Section 2 were greater than in
Section 1 (p ¼ 0.03) and in Section 3 (p ¼ 0.016) (Table S2†).
Deforestation oen leads to increased sediment loading to
waterways and downstream rivers by increasing surface
runoff.26,27
In the MDD region, ASGM activities have led to more
than 50 000 hectares of deforestation since 1999, which exceeds
forest loss from ranching, agriculture, and logging
combined.12,28
In the catchment area that feeds into the river
sampling sites of this study, much of the mining activity and
deforestation is localized within Section 2 and its major
tributaries as shown through satellite images from Asner et al.
2013 and mapping efforts by Asociaci´on para la Conservaci´on
de la Cuenca Amaz´onica. The increased TSS in Section 2 was
coincident with increased mining activity and likely indicates
mining in the region enhances sediment transport to down-
stream areas.
Suspended particulate mercury (HgP) generally represents the
major Hg transport mechanism throughout the river system.17–19
In
the MDD River surface water, HgP concentrations increased with
distance downstream through Section 2 (Fig. 3b, Table S3†),
similar to trends observed for Hg concentrations in the bottom
sediments. River Section 2 had an estimated average HgP
concentration that was 9.97 ng LÀ1
greater than in Section 1 (95%
C.I. 6.1, 13.8; p 0.001). Concentrations in Section 3 stabilized with
an estimated increase of 3.5 ng LÀ1
relative to Section 2 (95% C.I.
À0.2, 7.3; p ¼ 0.063; Table S2†). HgP concentrations were greater in
the March–April wet season and lower in the June–July dry season
(p 0.01) due to greater TSS concentration during the wet season
than the dry season (Fig. 3).
The increase of HgP with distance downstream, however, was
not simply due to increased TSS concentration in the water
column. In both seasons TSS decreased in Section 3 while HgP
remained relatively constant (the trends calculated for HgP in
Section 3 were not signicant, Fig. 3 and Table S1†). These
results suggest the existence of additional sources of Hg to the
region. Section 3 includes the capital city of the MDD region,
Puerto Maldonado, where TSS and HgP are likely inuenced by
urbanization, sewage discharge, and gold amalgam burning.
Further work should examine the inuence of urban releases to
TSS and HgP dynamics.
Other surface water quality parameters such as pH,
conductivity, temperature and dissolved oxygen did not vary
dramatically between sections or seasons, though some trends
were identied (Table S4†). From the upper watershed (Section
1) to mid-region and lower watershed (Sections 2 and 3),
temperature increased and dissolved oxygen concentrations
decreased during both seasons. This pattern was consistent
with conditions of atmospheric O2 saturation in the surface
water (p 0.01; Fig. S1†).
Collectively, these results of the surface water analyses
indicated that particulate Hg concentrations in the water
column were closely linked to suspended solids and Hg in the
river sediment, probably via particle settling and reentrain-
ment. However, differences in HgP concentrations between
Sections 2 and 3 were not explained simply by changes in TSS
concentrations in the river. In both the water column and
sediment, increased amounts of Hg concentrations coincided
with increased anthropogenic activities such as ASGM, defor-
estation, and agricultural expansion.
Hydrologic transport of mercury from large areas of mining
The Colorado and Inambari Rivers drain the largest areas of
active mining in the watershed and are major tributaries that
feed into the MDD River at km 221 and km 355, respectively
(Fig. 1).1,12
The surface water in these tributaries contained
signicantly higher total concentrations of particulate mercury
than in the MDD River, expressed as concentration in the water
(HgP) (Fig. S2†). Furthermore, the concentration of Hg stan-
dardized by total suspended solids mass (HgSS, mg Hg per kg
solids) was greater in the tributaries as compared to the MDD
River (Fig. S3†). The TSS in the major tributaries was generally
less than in the MDD River (Fig. S4†).
Fig. 3 (a) Total suspended solids (TSS) and (b) suspended particulate
Hg (HgP) from the surface water of the MDD River and major tributaries
during the two sampling events in 2013. Error bars indicate standard
deviation among triplicate field samples. The solid lines and dashed
lines represent linear splines for each section during the March/April
and June/July seasons, respectively. Regression analysis and spline
information available in Tables S1 and S2.†
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8. While HgP and HgSS values were greater in the tributaries,
HgP in the MDD River directly downstream of conuences with
Colorado and Inambari Rivers did not increase as compared to
the upstream (Fig. S2†). This was likely due to dilution of the
tributaries by the main river. For example during the June–July
sampling season, the ow rate in the MDD River was approxi-
mately 80 m3
sÀ1
at sites within 40 km upstream of the
conuence with the Colorado River (Fig. S5†). In contrast, the
Colorado River ow rate was approximately 10 m3
sÀ1
, indi-
cating that the Colorado was diluted by a factor of nine aer
joining the MDD River. At the Inambari River, the ow rate of
the tributary (120 m3
sÀ1
) was approximately equal to the MDD
River ow (140 m3
sÀ1
), representing a dilution of approximately
two upon entering the MDD River.
A mass balance of Hg inputs from the tributaries for the
June/July season was performed by comparing expected and
calculated HgP concentrations downstream of each conuence.
In all four tributary conuences, the observed and calculated
HgP values were consistent with each other (Fig. S6†), indicating
that the major input at this point in the MDD River was
captured by the tributary input.
While HgP concentrations did not appear to signicantly
change downstream of conuences, Hg loading rates from
these tributaries were relatively high, indicating a source of total
Hg to the river. Hg loading rates (calculated by multiplying ow
rate and HgP concentration) increased from 1.3 mg sÀ1
upstream of the conuence with the Inambari River (km 356) to
2.4 mg sÀ1
directly downstream (Fig. S7†). Likewise at the
conuence with the Colorado River (km 224), Hg loading rates
were 0.18 mg sÀ1
upstream and 0.37 mg sÀ1
downstream, a
doubling of Hg transport downstream. Additional monitoring
of the Inambari River is needed in order to identify specic
areas of direct Hg release from mining areas.
The Tambopata River drains from the Tambopata Reserve,
which until recently was a relatively protected region. In the past
ve years, mining has increased in the Malinowski River area,
which drains into the Tambopata River.12
While the Tambopata
River does not appear to contribute signicantly to Hg loading
(Fig. S7†), there was a dramatic increase of Hg loading down-
stream of the conuence. Puerto Maldonado is an urban center
located at the conuence of the Tambopata and MDD Rivers.
While mining occurs near Puerto Maldonado with less
frequency, Hg is actively used in gold shops to further purify ores
taken from the mining areas. Release of Hg and urban runoff
from both mining in the Malinowski River and Puerto Maldo-
nado may strongly impact Hg and suspended solids concentra-
tions in the MDD River in Section 3 near km 484. Further, as
discussed above, the factors controlling HgP and TSS in urban-
ized areas within the Amazon should be examined further.
Urban runoff, including direct release of sewage and erosion,
may have dramatic effects on local Hg dynamics in the rivers.
Mercury in sh tissue
Fish obtained from the sampling events included a wide variety
of species (Table S5†) and represented sh that are typically
eaten by local residents. In this study, 47 of 200 (24%) sh
samples, and 39 of 123 (32%) carnivorous sh samples excee-
ded the mercury guideline for human consumption set by the
World Health Organization (0.5 mg kgÀ1
). Moreover, 79 of 200
(40%) total sh samples and 59 of 123 (48%) in carnivorous sh
samples exceeded the US Environmental Protection Agency
(EPA) sh tissue based water quality limit of 0.3 mg Hg kgÀ1
of
sh, indicating severe water quality impairment.
Carnivorous sh species contained greater concentrations of
Hg than non-carnivorous sh (p 0.01). The higher trophic level
species demonstrated greater frequency for exceeding the WHO
standard for Hg. For example, the average Hg concentrations of
sabalo and chambira species were greater than 1 mg kgÀ1
of Hg
(Fig. 4), a threshold in which sh consumption is recom-
mended to be no more than once per month.29
For other species
including dorado, doncella, toa, and corvina, the average Hg
concentrations exceeded the WHO concentration guideline of
0.5 mg kgÀ1
. All of these sh species were omnivores or strict
carnivores and are expected to contain greater levels of Hg due
to food web biomagnication.
Mercury concentrations in the muscle tissue of the sh
increased with distance from the headwaters at Atalaya (km 1)
to sites further downstream (Fig. 5), and were signicantly
greater in Section 2 (km 181 to 400) than in Section 1 (p 0.001)
or Section 3 (p 0.001). Changes in mercury concentrations in
muscle tissue of the sh cannot fully be explained by sh
length, which might be a proxy for sh age. Mercury concen-
trations did not strongly correlate with sh length for carnivo-
rous or non-carnivorous species (PC 0.40; Fig. S8a†). For the
six species of sh with sample numbers equal to or greater than
10, Hg concentrations were not strongly correlated with length
(PC 0.5 in all cases; Fig. S8b and c†). Instead, for the non-
carnivorous species bocachico and yahuarachi, Hg concentra-
tions exceeded WHO standards only at sites near Boca Inambari
(km 355), a community directly downstream of dense mining
activity. The highest Hg concentration in a single sh was 2.8
mg kgÀ1
from a chambira caught within the river downstream of
mining at San Juan Grande (km 265).
Fig. 4 Average Hg concentrations in fish tissue (wet weight basis) for
18 commonly eaten fish collected from the Madre de Dios River. Error
bars represent the 95% confidence interval around the mean
concentration throughout the region. The green dashed line repre-
sents the WHO and Peru's Ministry of Health recommendation for safe
human consumption. The solid and bold dashed lines represent
weekly and monthly consumption guidelines from the US EPA.
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9. Fish mobility in the region is not well documented and may
contribute to the high variability of Hg concentrations among
sh tissue samples within sections. As indicated in Table S5,†
most of the sh species in this study are migratory (i.e. capable
of traveling more than 100 km during its lifetime). Non-
migratory sh accounted for 48 of 200 (41 of 123 carnivorous)
sh samples. An analysis of Hg concentration in sh was per-
formed for the non-migratory sh, and the outcome also
demonstrated increased concentrations in Sections 2 and 3
relative to Section 1 (Fig. S9†). However, the condence intervals
were relatively large due to small sample size.
Mercury release in the MDD and implications for
bioaccumulation
Mercury concentrations in the MDD River sediments were
approximately one order of magnitude lower than Hg concen-
trations reported for other regions with ASGM activities, such as
in Brazil (41 to 346 ng gÀ1
),30
Guyana (29 to 1200 ng gÀ1
),31
Suriname (130 to 220 ng gÀ1
),32
and the La Rinconada Mine
Complex in Peru (up to 232 000 ng gÀ1
).33
Concentrations were
more similar to regions not directly impacted by ASGM,
including the Tambopata River in the MDD region in 2009 (13
ng gÀ1
),34
and Veracruz State, Mexico (27.5 to 90.5 ng gÀ1
).35
Despite relatively low concentrations of Hg in sediment and
suspended solids within the MDD River, sh tissue concentra-
tions in the central and lower region were in the same range or
higher than regions with greater total Hg in sediment.30,32,33
The benthic ecosystem in the central and lower region of the
MDD River may be areas of high net MeHg production relative
to portions near the headwaters of the river (as indicated by
geographical trends in %MeHg values, Fig. 2c). Studies have
shown that Hg aging in sediments over days and weeks result in
less reactive and bioavailable Hg forms such as HgS minerals
when compared to newer sources such as Hg freshly deposited
from the atmosphere or released into the river as dissolved
Hg.5,36
In regions with high rainfall, Hg inputs from landscape
runoff can contribute to increasing ‘new’ sources of Hg in
waterways before it is able to be sequestered in soil.37
While the
results of this study indicated that Hg was transported from the
mining sites to the MDD River via the Colorado and Inambari
Rivers, the reactivity and methylation potential of this mercury
needs to be further explored, particularly in relation to naturally
occurring Hg, and Hg that deposited onto the landscape via
atmospheric deposition and reached the river via landscape
drainage. If Hg directly released to waterways from ASGM is
highly bioavailable for methylating bacteria, then this source of
Hg may have a greater risk for methylation and bio-
accumulation than Hg from native or natural sources.
Risks for dietary exposure to mercury
Mercury concentrations in sh from the MDD River were used
to calculate probabilities of dietary Hg exposure exceeding
public health guidelines. For communities located in Section 2,
the risk of consuming sh that exceed the 0.5 mg kgÀ1
WHO
threshold is greater than in other two sections of the MDD
River. Between Tambo Blanquillo and Laberinto (km 181 to
400), 55% of the carnivorous sh samples contained Hg
concentrations exceeding 0.5 mg kgÀ1
as compared 6%
exceeding in Section 1 and 24% in Section 3 (Table 2). In Lago
Valencia (a large oxbow lake that receives water from and drains
into the MDD River at km 545), concentrations of Hg in sh
tissue were also high relative to Sections 1 and 3 of the MDD
River. Average carnivorous sh tissue concentrations from Lago
Valencia did not differ signicantly from Section 2 (p ¼ 0.39,
Fig. S10†).
The observed sh Hg concentrations in the MDD River
indicated that consumption of carnivorous sh must be limited
in order to avoid excessive Hg body burdens. Residents living in
Section 2 of the MDD River who consume two carnivorous sh
meals weekly would likely exceed the United Nations Environ-
ment Program (UNEP) provisional tolerable weekly intake
(PTWI) of 1.6 mg per kg body weight (bw) for pregnant women
and the PTWI of 3.2 mg per kg bw for children and women of
childbearing age (Fig. 6). In order to avoid exceeding the 1.6 mg
per kg bw PTWI, pregnant women should consume fewer than 2
carnivorous sh meals per week in Sections 2 and 3 (Fig. S11†).
Children living in the region who consume two carnivorous sh
per week would have an approximate body burden of 5 mg per kg
bw, which exceeds the 3.2 mg per kg bw. In contrast, children
living in communities near the headwaters (Section 1) can
consume nearly 5 carnivorous sh meals per week without
exceeding health guidelines. With the exception of Section 2,
children throughout the watershed can consume at least two
non-carnivorous sh meals.
The concentrations of Hg in carnivorous sh tissue may be a
public health risk in the region, especially in the downstream
regions occupied by Section 2 of the MDD River. Given the level
of Hg bioaccumulation in sh in MDD, it is imperative to
quantify the Hg exposure for residents. The risk of dietary
Hg exposure must also be balanced with the health
benets of sh consumption, such as improved childhood
Fig. 5 Total Hg concentrations in carnivorous and non-carnivorous
fish muscle tissue (mg kgÀ1
, wet weight) collected from the main stem
of the Madre de Dios River in 2013. 95% confidence intervals around
the mean fish concentration within each section are represented by
red, solid boxes for carnivorous fish and blue, dashed boxes for non-
carnivorous fish. The WHO limit (solid line) for human consumption
(0.5 mg per kg Hg) is based on human health threshold for weekly
consumption. The US EPA Criterion (dashed line) is based on a fish
tissue based water quality criterion (0.3 mg per kg MeHg).
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10. neurodevelopment.38
The US EPA recommends approximately
two sh meals per week for omega-3 fatty acids. In the MDD
region, consumption of non-carnivorous sh may provide
health benets while also minimize Hg exposure risk. However,
risk from mercury consumption may still be present for chil-
dren in communities located in Section 2 of the MDD River
(Fig. 6). Future work must assess Hg exposure and health
outcomes in the MDD region so that the health risks of dietary
Hg exposure can be appropriately identied.
Conclusions
This study is the rst, to the best of our knowledge, to identify a
gradient of increasing Hg contamination and food web accu-
mulation over a relatively broad geographical range where
ASGM is prevalent. Rivers draining major ASGM mining areas,
Huepetuhe and Guacamayo, are an important source of
mercury loading to the MDD River. Future research should
specically address mercury reactivity and transport from
ASGM sites to determine how to best curb environmental and
human health impacts.
While the direct human health risks of Hg from ASGM
activity are relatively well known, many studies focus closely on
direct Hg exposure to miners without examining exposure to
non-miners with distance or density of mining activity.2,39
It is
clear from other studies that exposure during amalgamation
and burning are extremely hazardous.3,9,10
This study is one of
the rst to show signicant health risks to communities not
directly involved in mining through sh consumption and
mercury accumulation in downstream regions. Children living
within the central portion of the watershed cannot safely
consume carnivorous sh without exceeding recommended
international Hg body burdens. The health risks of consuming
certain sh in the central and lower portions of the MDD
watershed must be communicated to communities. The
regional health directorate, Direction Regional de Salud (DIR-
ESA), is uniquely positioned to disseminate this information to
local residents.
In the Madre de Dios region, deforestation and mercury
release are an immediate threat to both local and distant
downstream communities, many of which do not benet
economically from ASGM. Policies are needed to simulta-
neously decrease atmospheric Hg releases from gold amalgam
burning, sediment mobilization from deforestation, and direct
releases of Hg to the river from large areas of mining activity.
Demand for gold has existed for millennia and is not likely to
decrease in the near future. Realistic approaches are needed to
balance the need for wealth accumulation among some of the
poorest communities in the region and environmental stew-
ardship, rather than the aggressive military efforts that attack
individual mining operations. Governments need to facilitate
the establishment of legal mining operations that integrate Hg
capture systems, environmental remediation, and health
monitoring that enhances community-based cooperation and
provides residents in Madre de Dios a viable pathway toward
sustainable human and environmental health.
Acknowledgements
This research was funded by the Duke Global Health Institute,
the Pratt School of Engineering, the Bass Connections Program,
and the Center for Latin American and Caribbean Studies at
Duke University. Additional support was provided by the Inter
American Institute for Global Change Research Grant
#CRN3036. The local health directorate, Direccion Regional de
Salud (DIRESA), Peruvian Navy, United States Naval Medical
Research Unit (NAMRU-6), and Asociaci´on para la Conservaci´on
de la Cuenca Amaz´onica (ACCA) provided invaluable logistical
support for this project. The Duke Global Health Bass
Connections Team in Peru assisted in eld collection of data
during June/July 2013. We thank Crissel Vargas, Jaime Villamar
and Cecilio Huamantupa for their assistance in eld data
collection, and Lauren Riedle, Laura Rogers, and Kaitlyn Porter
for their assistance with mercury analyses.
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