Environmental Pollution 231 (2017) 262e270

Contents lists available at ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Mercury contamination level and speciation inventory in Lakes

Titicaca & Uru-Uru (Bolivia): Current status and future trends*
S. Gue
dron a, b, *, D. Point c, d, **, D. Acha d, ***, S. Bouchet e, P.A. Baya c, E. Tessier e,
M. Monperrus e, C.I. Molina d, A. Groleau f, L. Chauvaud g, J. Thebault g, E. Amice g,
L. Alanoca b, C. Duwig h, G. Uzu h, X. Lazzaro d, i, A. Bertrand j, S. Bertrand j, C. Barbraud k,
K. Delord k, F.M. Gibon i, C. Ibanez l, M. Flores b, d, P. Fernandez Saavedra d, M.E. Ezpinoza d,
C. Heredia d, F. Rocha d, C. Zepita d, D. Amouroux d, e, ****
a
Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, IRD, IFSTTAR, ISTerre, 38000 Grenoble, France
b
Laboratorio de Hidroquímica, Instituto de Investigaciones Químicas, Universidad Mayor de San Andr
es, Campus Universitario de Cota-Cota, Casilla 3161,
La Paz, Bolivia
c

Geosciences Environnement Toulouse, UMR5563 - IRD UR 234, Universit
e Paul Sabatier, 14 Avenue Edouard Belin 31400 Toulouse, France
d
Unidad de Calidad Ambiental (UCA), Instituto de Ecología, Universidad Mayor de San Andr
es, Campus Universitario de Cota Cota, Casilla 3161, La Paz,
Bolivia
e
CNRS, Univ. Pau & Pays Adour, Institut des sciences analytiques et de Physico-chimie pour l’Environnement et les Mat
eriaux, MIRA, UMR5254, 64000 PAU,
France
f
Institut de Physique du Globe de Paris (IPGP), 1, rue Jussieu, 75238 Paris Cedex 05, France
g
Laboratoire des Sciences de l’Environnement Marin (LEMAR), UMR 6539, IUEM Technopo ^le Brest-Iroise, rue Dumont d'Urville, 29280 Plouzan
e, France
h
Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, IRD, IFSTTAR, IGE, 38000 Grenoble, France
i
Biologie des Organismes et Ecosyst emes Aquatiques (BOREA), Institut de Recherche pour le D
eveloppement (IRD), UMR 7208, Paris, France
j
MARine Biodiversity, Exploitation and Conservation (MARBEC), Institut de Recherche pour le D
eveloppement (IRD), Univ. Montpellier, Place Eug
ene
Bataillon, ba^t 24, CC093 34 095 Montpellier Cedex 5, France
k
Laboratoire du Centre d'Etudes Biologiques de Chiz
e (CEBC), UMR 7372, CNRS, Universit
e de La Rochelle 405 Route de La Canauderie, 79360 Villiers-en-
Bois, France
l
UPA, Universidad Pública de El Alto, Ecología y Recursos Naturales, El Alto, Bolivia

a r t i c l e i n f o a b s t r a c t

Article history: Aquatic ecosystems of the Bolivian Altiplano (~3800 m a.s.l.) are characterized by extreme hydro-climatic
Received 16 May 2017 constrains (e.g., high UV-radiations and low oxygen) and are under the pressure of increasing anthro-
Received in revised form pogenic activities, unregulated mining, agricultural and urban development. We report here a complete
27 July 2017
inventory of mercury (Hg) levels and speciation in the water column, atmosphere, sediment and key
Accepted 2 August 2017
sentinel organisms (i.e., plankton, fish and birds) of two endorheic Lakes of the same watershed differing
Available online 12 August 2017
with respect to their size, eutrophication and contamination levels. Total Hg (THg) and mono-
methylmercury (MMHg) concentrations in filtered water and sediment of Lake Titicaca are in the lowest
Keywords:
Mercury
range of reported levels in other large lakes worldwide. Downstream, Hg levels are 3e10 times higher in
Water the shallow eutrophic Lake Uru-Uru than in Lake Titicaca due to high Hg inputs from the surrounding
Sediment mining region. High percentages of MMHg were found in the filtered and unfiltered water rising up from
Biota <1 to ~50% THg from the oligo/hetero-trophic Lake Titicaca to the eutrophic Lake Uru-Uru. Such high %
Titicaca MMHg is explained by a high in situ MMHg production in relation to the sulfate rich substrate, the low
oxygen levels of the water column, and the stabilization of MMHg due to abundant ligands present in
these alkaline waters. Differences in MMHg concentrations in water and sediments compartments be-
tween Lake Titicaca and Uru-Uru were found to mirror the offset in MMHg levels that also exist in their
respective food webs. This suggests that in situ MMHg baseline production is likely the main factor

*
This paper has been recommended for acceptance by Prof. W. Wen-Xiong.
* Corresponding author. Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, IRD, IFSTTAR, ISTerre, 38000 Grenoble, France.
** Corresponding author. Ge
osciences Environnement Toulouse, UMR5563 - IRD UR 234, Universite
Paul Sabatier, 14 Avenue Edouard Belin 31400 Toulouse, France.
*** Corresponding author.
**** Corresponding author. Unidad de Calidad Ambiental (UCA), Instituto de Ecología, Universidad Mayor de San Andre
s, Campus Universitario de Cota Cota, Casilla 3161, La
Paz, Bolivia.

dron), [email protected] (D. Point), [email protected] (D. Acha), [email protected] (D. Amouroux).
E-mail addresses: [email protected] (S. Gue

http://dx.doi.org/10.1016/j.envpol.2017.08.009
0269-7491/© 2017 Elsevier Ltd. All rights reserved.
 S. Gu
edron et al. / Environmental Pollution 231 (2017) 262e270 263

controlling MMHg levels in fish species consumed by the local population. Finally, the increase of
anthropogenic pressure in Lake Titicaca may probably enhance eutrophication processes which favor
MMHg production and thus accumulation in water and biota.
© 2017 Elsevier Ltd. All rights reserved.

1. Introduction species are compared with previous studies performed in large or

elevated lakes. Biogeochemical and anthropogenic factors influ-
The Bolivian Altiplano is one of the largest high plateaus in the encing the sources, distribution and speciation of Hg in the
world containing two large lakes, Lake Titicaca in the north part different limnological compartments and selected sentinel organ-
and Lakes Uru-Uru/Poopo
in the central part of an endorheic sys- isms are discussed. Based on these discussions and the observed
tem consisting in the Titicaca-Desaguadero-Poopo
-Coipasa Salt spatial gradients in the ecosystem, we finally propose scenarii of
Lake (Revollo, 2001; Delclaux et al., 2007). Lake Titicaca is the most possible future trends in Hg species levels and their impacts on this
important water resource of the Andean Altiplano, a major source ecosystem.
of fish for ~3 million people and the largest navigable water body in
the world lying at an altitude of 3809 m above sea level (a.s.l.). Its 2. Material and methods
ecological functioning and limnology have been widely investi-
gated between 1980 and 2000 (Collot et al., 1983; Pourchet et al., 2.1. General settings
1994; Mourguiart et al., 1998; Dejoux, 1992). Nowadays, the
ecological equilibrium of the region is disturbed by a recent but 2.1.1. Lake Titicaca
very intensive urban demography and the intensification of mining Lake Titicaca (Fig. 1a) comprises of two nearly separate basins:
activities, fisheries and agriculture around the Lake. For example, the great lake named “Lago Mayor” or “Lago Chucuito” (7131 km2;
Puno Bay, on the Peruvian side of Lake Titicaca, has been identified mean depth ¼ 100 m; max depth ¼ 285 m) and the smaller lake
as a contaminated area by urban and industrial effluents since the named “Lago Menor” or “Lago Huin ~ aimarca” (1428 km2; mean
1980's (NorthCote et al., 1989). The most preoccupying issue on the depth ¼ 9 m; max depth Chua trough ¼ 40 m) (Dejoux, 1992). The
Bolivian side of the Lake (Lago Menor e southern basin of the lake) two basins are connected by the Strait of Tiquina and a single outlet
is the extremely rapid development of El Alto city, which popula- for the lake, the Río Desaguadero, which drains out the southern
tion increased from 95,000 inhabitants in 1976 to around 1.2 end of Lago Menor to the central Altiplano (i.e., to Lakes Uru-Uru
million according to the last census (Mazurek, 2012) with minimal and Poopo
) (Cross et al., 2000; Dejoux, 1992). Because of its
land planning. Wastewater from El Alto city, its facilities, manu- geographical location and high altitude (3809 m a.s.l.), Lake Titicaca
factures and small scale industries, are discharged in the Katari is subject to the tropical zone climate (rainy season concentrated
river, which flows to the Lago Menor with less than 50% of water between December and March) and its hydrological regime is
treated (Chudnoff, 2009). Among the emitted pollutants (e.g., nu- dominated by evaporation (~95%) while rivers outflow repre-
trients, traces metals and organic contaminants) (Duwig et al., sents ~ 5%. The resulting Lake water is alkaline with a salinity close
2014; Archundia et al., 2017), mercury (Hg) contamination is one to 1 g L
1 (Dejoux, 1992). Sediments of Lake Titicaca are covered
of the preoccupying issues in this fragile ecosystem. So far, only with Totoras (Schoenoplectus Californicus) in the inner margin
three studies focused on Hg contamination in the coastal areas of (0e2 m depth) and by macrophytes (mostly Characeae spp.) in the
the great Lake Titicaca (Gammons et al., 2006; Molina and Point, photic zones (i.e.,~15 m depth) with maximum development be-
2014; Monroy et al., 2014) revealing high Hg concentrations in all tween 4.5 and 7.5 m. Macrophytes constitute more than 60% of the
fish species collected in the northern part of the Lago Mayor, total biomass in Lago Menor (Dejoux, 1992) and colonize a third of
particularly at the Mouth of the Ramis River (up to 1840 ng g
1 THg, its bottom (~436 km2) between 2 and 15 m in depth (Collot et al.,
dw in Orestias agassii) where intense gold mining activities are 1983). Major sources of anthropogenic Hg, the gold mining cen-
documented. Hg levels in fish muscle from other coastal areas of ters, are identified at the mouth of the Ramis and Suchez rivers
the Lago Mayor where found below regulatory health guidelines. (Fig. 1a). Two other urban wastewater sources to the lake are
No data exists yet in Lago Menor which is considered as the most located in the Puno Bay (Lago Mayor) and Cohana Bay (Lago Menor)
productive area and is also impacted by anthropogenic inputs. originating from Puno and El Alto cities, respectively (Fig. 1a).
Downstream Lake Titicaca, Lake Uru-Uru, a man-made reservoir,
combines diverse metal and organic pollutions since it receives 2.1.2. Lake Uru Uru
important discharges from urban and mining activities. Recently, Lake Uru Uru is located in the central part of the Bolivian Alti-
several studies evaluating Hg contamination in Lake Uru-Uru have plano region (Fig. 1b), south to Oruro city where numerous mining
highlighted high concentrations and percentages of toxic MMHg in (e.g., Au, Ag and Sn) and smelting activities are concentrated. This
the water column and biota (Molina, 2015; Alanoca et al., 2016a, shallow aquatic ecosystem is a man-made reservoir supplied
2016b; Lanza et al., 2016). mainly by the Rio Desaguadero waters. The Lake surface and depth
In this paper, we report for the first time, a complete inventory vary between 120 and 350 km2 and 0.25e1 m, respectively, as
of Hg levels and speciation, including inorganic Hg(II), elemental function of the seasons. Fishing activities are practiced year round
Hg (Hg0) and mono-methylmercury (MMHg), from samples and are an important protein and financial resource for local
collected between 2010 and 2016 in the different compartments of communities. A strong contrast exists between the Northern and
Lake Titicaca and Uru-Uru. Hg was measured in the atmosphere Southern parts of the lake, with higher density of sedge (Schoeno-
(total gaseous Hg - TGM), atmospheric fallouts (i.e., filtered and plectus totora), grass (Ruppia spp.) and algae (Characeae) in the
particulate Hg), water column (i.e., filtered, particulate and dis- southern part (Tapia and Audry, 2013). Previous investigation
solved gaseous Hg), sediment (i.e., porewater and solid particles) (Alanoca et al., 2016a) studying 24 h biogeochemical cycles
and biota (i.e., plankton, fish and birds). Concentrations of Hg demonstrated that diurnal variability (e.g., temperature, oxygen) in
264 S. Gu
edron et al. / Environmental Pollution 231 (2017) 262e270

Fig. 1. Map of the Bolivian Altiplano Titicaca-Desaguadero-Poopo
-Coipasa Salt Lake (TDPS basin) hydrosystem with (a) Lake Titicaca (Lago Mayor) (b) Lake Titicaca (Lago Menor) and
(c) Lake Uru-Uru. Sampling sites (site codes) are for (a) Lake Titicaca, BE: Escoma Bay; IL: Isla de la Luna; IS: Isla del Sol; CH: Chua; HU: Huatajata, BCin: Cohana Bay (inside the bay)
and BCout: Cohana Bay (outside the bay) and (b) Lake Uru-Uru: UU12: Uru-Uru.

Lake Uru-Uru can overwhelm seasonal variations with higher daily fisherman using gillnets. Blood samples from two water bird spe-
gradients found during the dry season. Furthermore, the synergistic cies were collected using reference sampling protocols available
effect of mining (i.e., acid mine drainage (AMD)) and urban efflu- elsewhere (Molina and Point, 2014). Mercury concentrations in
ents to this shallow lake was proved to enhance Hg methylation food web samples are expressed on a dry weight basis.
with the sediment being the main source of MMHg during the dry Dissolved gaseous Hg (DGM), Filtered (F) and UNFiltered (UNF)
season (Alanoca et al., 2016b). total mercury concentrations (THg) in surface and pore waters were
determined by cold vapor atomic fluorescence spectrometry (CV-
2.2. Sampling location, strategy and elemental analysis AFS) after conversion of all mercury species into Hg0 followed by
detection using a Tekran® (Model 2500) (Bloom and Fitzgerald,
Details on the sampling, site location and analytical protocols 1988; Cossa et al., 2009; Gue
dron et al., 2015). DGM was analyzed
are given in the supplementary information 1 (S.I.1 and 2) and in by thermodesorption (600  C) and CV-AFS.
Alanoca et al. (2016a). Briefly, surface water samples were collected THg concentrations in sediment and biota were determined by
during 7 main campaigns performed between 2010 and 2016. atomic absorption spectrophotometry after dry mineralization and
Water sampling was performed with a Teflon-coated Go-Flo trace gold amalgamation (Altec, Model AMA 254 and Millestone,
metals sampler and stored unfiltered (UNF) or filtered (F) (0.22 mm DMA80).
PVDF) immediately after sampling. All water samples were stored Filtered monomethylmercury (MMHgF) concentrations were
in acid-washed FEP Teflon containers and acidified with HCl (0.5%, analyzed using an ethylation purge and trap-gas chromatograph-
v/v, Ultrex grade - Baker). Dissolved gaseous mercury (DGM) was AFS analyzer (MERX System, Brooks Rand®) and a propylation ID-
collected in situ from unfiltered water samples, purged within GCeICPMS (Monperrus et al., 2008; Bouchet et al., 2013; Gue
dron
~0.5 h after sampling and collected on a goldecoated sand traps. et al., 2014; Sharif et al., 2014). For solids, MMHg was extracted
Total gaseous mercury (TGM) and atmospheric fallouts were from ~100 mg of solid samples with 5 mL HNO3 (6 N) at 60  C for
collected on the shore of Lago Menor at Huatajata, nearby the 2 h. Digestion aliquots were then analyzed in duplicates and
meteorological station (Fig. 1a and S.I.2). Surface sediments were quantified using the standard addition technique.
recovered using a gravity corer. Cores were immediately extruded Dissolved organic carbon concentrations (DOC) were deter-
and sediment was collected in centrifuge vials, N2-flushed and mined using a Non Dispersive Infra-Red (NDIR) CO2 Shimadzu®
centrifuged at 4000 r.p.m. for 20 min. For each sediment sample, (Model VCSN) spectrometer after humid oxidation in a sodium
the supernatant (i.e. porewater) was filtered (0.45 mm, PVDF) into persulfate solution at 100  C.
20 ml Teflon vials and acidified with HCl Ultrex. Biological samples
representative of the aquatic food webs were collected in Lago 2.3. Statistical analyses
Menor (Titicaca) and lake Uru-Uru mostly during the late dry sea-
son period (OcteNov). Zooplankton samples were collected using Statistical analyses were performed using JMP® software (SAS
nets (Molina et al., 2010) and fish samples were collected by local Institute, USA). One-way ANOVA were performed when comparing
 S. Gu
edron et al. / Environmental Pollution 231 (2017) 262e270 265

two datasets. Homogeneity of variances were tested using the 3.2. Hg spatial distribution, speciation and partitioning in surface
Brown-Forsythe test. In the case of unequal variances, a Welch sediments
ANOVA test was used.
THg concentrations in surface sediments of Lake Titicaca were
variable between sites (Table 2) with lowest concentrations found
3. Results and discussions
in shallow (water column depth between 2 and 15 m - HU:
average ± SD: 19 ± 4 ng g
1) and very shallow (water column
3.1. Mercury speciation in air and atmospheric fallouts of Lake
depth < 2 m e BCin: 38 ± 13 ng g
1) coastal areas of the Lago Menor
Titicaca
and highest concentrations in the deep sites of the lake (IS and CH:
77 ± 34 ng g
1). These values are in the higher range of reported
Total gaseous mercury (TGM) concentrations in air on the shore
THg concentrations for high altitude Tibetan lake but in the lower
of Lake Menor were not significantly (p > 0.05) different between
range for other great lakes worldwide (Table 2). MMHg concen-
the end of the wet (1.11 ± 0.23, N ¼ 1407) and of the dry season
trations in sediments also varied between sites and never exceeded
(0.82 ± 0.20 ng m
3, N ¼ 1037). Measured TGM concentrations
4% of THg. The highest concentrations and percentages were found
were in the lowest range of the background concentrations
in coastal contaminated sites (BCin: 0.98 ± 0.50 ng g
1 and
(Table 1) reported for the northern (1.5e2.5 ng m
3) and for the
2.2± 1.1%, BE: 1.1 ± 0.3 ng g
1 and 1.6 ± 0.2%) and shallow sites (HU:
southern hemispheres (mean GEM: 0.84e1.09 ng m
3) (Meuleman
0.66 ± 0.08 ng g
1 and 3.5 ± 0.5%) followed by deep sites (CH:
et al., 1995; Lin and Pehkonen, 1999; Vette et al., 2002; Campbell
0.51 ± 0.01 ng g
1 and 0.5 ± 0.1%) while the lowest were found in
et al., 2003a; Cohen et al., 2004; Ryaboshapko et al., 2007; Baya
very shallow pristine areas (BCout: 0.07 ng g
1 and 0.3%). THg
and Van Heyst, 2010; Sprovieri et al., 2016). Such low TGM values
concentrations in sediment of Lake Uru-Uru were 5e10 time higher
suggest little influence of regional urban or industrial activities
than in Lake Titicaca illustrating the great impact of mining and
(e.g., La Paz/El Alto cities) atmospheric emissions. Except for the
urban effluent inputs to this shallow lake. MMHg in sediment of
cement factory in the city of Viacha, there is no combustion process
Lake Uru-Uru covered a large range of concentrations
nor industrial process using Hg reported in the region.
(1.09 ± 1.93 ng g
1) but exhibit relatively low percentage MMHg
THg measured in rain and fallouts sampled at lake Menor
(i.e., 0.7 ± 1.1%) which are in the same range as for coastal
(Table 1) were in the same range of reported concentrations for
contaminated sites of Lake Titicaca.
Lake Victoria (Campbell et al., 2003a) and for the great lake region
MMHg distribution in sediment porewater (MMHgPW) showed
(Hall et al., 2005; Risch et al., 2012). THg concentrations in unfil-
different distribution than for sediment matrix with highest con-
tered fallouts samples (THgUNF) were twice those in filtered sam-
centrations measured in shallow and very shallow sites
ples (<0.45 mm), suggesting that particulate matter (>0.45 mm)
(5.8 ± 5.6 ng L
1) rising up to 12.2 ng L
1 at HU site (sediment
contributes to almost 50% of Hg deposition in fallouts. Filtered
covered by Characeae and biofilms) and lowest in the deep sites
MMHg concentrations (0.11 ± 0.06 ng L
1) represented 5.0 ± 3.8% of
(CH: 0.84 ± 0.23 ng L
1). Interestingly, elevated % MMHg was
filtered THg levels in fallouts and were within reported range for
encountered at almost all sites reaching 47 ± 26% in very shallow,
concentrations and %MMHg in precipitations collected in the great
39 ± 27% in shallow sites and 23 ± 15% in deeper sites. Highest
lake region and elsewhere (Bloom and Watras, 1989; Hall et al.,
MMHgPW concentrations were encountered particularly in the
2005; Graydon et al., 2008). Although the sources of the MMHg
shallow carbonate sediments (e.g., HU) where high sulfate contents
measured in fallouts are difficult to diagnose, the presence of
in both sediment and water (~250 mg L
1 - (Iltis et al., 1992)) are
MMHg in rain water is likely the result of a combination of the
likely the major drivers for Hg methylation by sulfate reducing
mechanisms occurring in the atmosphere at a regional scale (i.e.
bacteria (SRB), the most probable Hg methylators in such envi-
atmospheric Hg methylation (Gardfeldt et al., 2003; Malinovsky
ronments (King et al., 1999; Acha
et al., 2010; Parks et al., 2013).
and Vanhaecke, 2011; Yin et al., 2012) and in a minor extent the
An opposite trend is observed for Hg distribution between
photochemical transformations of liberated dimethylmercury
sediment porewater and solid phase and we suggest it is related
(DMHg) to the atmosphere to MMHg (Bloom and Watras, 1989;
both to the nature of sediment matrix (e.g., OM vs carbonate) and to
Prestbo and Bloom, 1995) with the Amazonian side as the major
different sedimentation rates amongst sites. Firstly, sediment
source since most of the rain originates from this region (Roche
enriched in OM (i.e., deep and very shallow sites - Rodrigo and
et al., 1992).

Table 1
Comparison of filtered and unfiltered total mercury (THg), filtered monomethylmercury (MMHg) in atmospheric depositions and total gaseous mercury (TGM) concentrations,
measured at Huatajata station, in Lake Titicaca with literature data for world's great lakes. Superscripts (a & b) refer to bibliographic reference (right column) from which data
originate.

Area Altitude Sampling period TGM (ng m
3) THgF (ng L
1) THgUNF (ng L
1) MMHgF (ng L
1) Reference
(m a.s.l)

Titicaca 3809 2013e2016 0.74e2.67 1.38e7.14 2.60e13.7 0.03e0.21 This study

(Lago Menor) (N ¼ 1407)a (N ¼ 14) (N ¼ 10) (N ¼ 12) (a late wet season and b

(mean ¼ 1.11 ± 0.23)a (2.96 ± 1.75) (mean ¼ 5.9 ± 3.07) (mean ¼ 0.11 ± 0.06) late dry season)
0.51e1.35
(N ¼ 1037)b
(mean ¼ 0.82 ± 0.20)b
Lake Victoria 1133 1994/95a & 1999b 1.05e1.52a 1.8 1e3.0b Campbell et al. (2003a, 2003b)a
Lake Baïkal 456 1992e1993a 0.73e6.1 2e21 0.1e0.25 Meuleman et al. (1995)a
Great Lakes region ~180 1998e2003 1e130 0.01e0.85 Hall et al. (2005)
Lake Michigan 176 1993a, 1994-1995a,b 1.5e3.6b 5.08 ± 1.55a 21.6 ± 13.9a 0.10 ± 0.10 a
Lamborg et al. (2002)a,
Vette et al. (2002)b
266 S. Gu
edron et al. / Environmental Pollution 231 (2017) 262e270

Table 2
Comparison of total mercury (THg) and monomethylmercury (MMHg) concentrations in sediment and filtered porewater Lake Titicaca and Uru-Uru with literature data for
world's great lakes. Superscripts (a & b) refer to bibliographic reference (right column) from which data originate.

Area Altitude Period THgsed THgPW MMHgsed MMHgPW Reference

(m a.s.l) (ng g
1) (ng L
1) (ng g
1) (ng L
1)
(% MMHg) (% MMHg)

Titicaca e Lago Mayor 3809 2013e2015 45e79 N.A. 0.93e1.36 N.A. This study
(1.6 ± 0.2%)
Titicaca e Lago Menor 3809 2013e2015 16e114 2.9e17.6 0.51e1.33 0.67e12.2 This study
(1.8 ± 1.5%) (37 ± 22%)
Lake Uru-Uru 3686 2010e2011 79e404 2.4e239.1 0.17e7.9 0.04e35.8 This study
(0.7 ± 1.1%) (30 ± 44%)
Tibetan Lakes 2813e4652 2006e2007 8e67a,b Wang et al. (2010)a; Yang (2010)b
Lake Victoria 1133 1990e1995a,b 74e450 a,b 5e85.5 0.18e0.24 0.21e2.54 b
Ramlal et al. (2003)a; Campbell et al. (2003a, 2003b)b
Lake Superior 180 1988a & 2000b 4e380 a,b DL - 780 a
2.15e6.45 b
Matty and Long (1995)a; Rolfhus et al. (2003)b
Lake Michigan 176 1988a & 1994e1995b 2e450 a,b DL - 220 a
0.01e0.45 b
Matty and Long (1995)a; Mason and Sullivan (1997)b

Wirrmann, 1992) show the highest sorption capacity for Hg and concentrations in the heterotrophic Lago Menor (Fig. 2). The
MMHg as illustrated by high partition coefficients (i.e., logKD ¼ log average particulate THg (THgUNF - THgF) in surface water repre-
[Hg]sed - log[Hg]PW) found at CH (logKD THg ¼ 4.42 ± 0.23, logKD sented 39± 16%, 46± 23% and 50± 20% of THgUNF measured in Lago
MMHg ¼ 2.79 ± 0.12) and BCin (logKD THg ¼ 3.78 ± 0.24, logKD Menor, Lago Mayor and lake Uru-Uru, respectively (S.I.3), showing
MMHg ¼ 2.45 ± 0.22). The lower Hg content in very shallow sedi- that almost half of THg is present as truly dissolved or colloidal Hg.
ment results from the high sedimentation rates (0.22e1 cm yr
1 - THg and MMHg concentrations in filtered and unfiltered water also
(Binford et al., 1992; Pourchet et al., 1994) due to large local OM vary with depth along the water column due to the variable
production and catchment inputs trapped in the dense totoras abundance and distribution of plankton (S.I. 4) that act as carrier
cover which contributes to almost 95% of the sedimentation phase for Hg. Mean MMHgF concentrations in Lago Mayor
(Pourchet et al., 1994). In deep areas, higher Hg concentrations (0.008 ± 0.006 ng L
1; 0.8 ± 0.4 %THg) and Lago Menor
results from a 10 to 50 times lower sedimentation rate (0.035 ± 0.044 ng L
1; 13 ± 26 %THg) were within the range of
(0.05e0.1 cm yr
1 - unpublished data) of OM originating from reported values for Baikal (Meuleman et al., 1995) and Laurentian
decomposition of plankton which are known to scavenge Hg from (Mason and Sullivan, 1997; Rolfhus et al., 2003) Lakes. Highest
the water column (Mason and Jenkins, 1995). Secondly, carbonate MMHgF concentrations were found in shallow coastal areas such as
rich (~60% CaCO3 - (Rodrigo and Wirrmann, 1992)) sediment in Cohana Bay where MMHgF represented 26± 30% of THgF. Despite
shallow areas exhibit the lowest Hg concentrations and logKD at HU lower MMHgF concentrations in Lake Titicaca water, their relative
and BCout (mean ± SD ¼ 2.81 ± 0.65 and 2.43 ± 0.65 for THg and abundance in the THg fraction is much more elevated compared to
MMHg, respectively) due to the weak affinity of Hg for carbonate other great lakes where %MMHg rarely exceed 1% (Table 3).
matrix (Gue
dron et al., 2013) and high sedimentation rates Downstream, THgF, THgUNF, MMHgF and MMHgUNF in surface wa-
resulting from large Characeae spp. production (Binford et al., 1992; ters of the shallow eutrophic Lake Uru-Uru were 3e10 times higher
Pourchet et al., 1994). Finally, the Hg contaminated and OM rich than those measured in Lake Titicaca (Fig. 2). Particularly high %
sediments of Lake Uru-Uru (Alanoca et al., 2016b) illustrate similar MMHg (44± 53% of THg) in Lake Uru-Uru highlights high produc-
characteristics as for OM rich sediments of Lake Titicaca with a high tion and accumulation of MMHg in this urban and mine impacted
Hg storage capacity as illustrated by higher logKD ecosystem (Tapia and Audry, 2013; Alanoca et al., 2016a).
(mean ¼ 4.45 ± 0.84 and 2.86 ± 1.59 for THg and MMHg, When data from both lakes are gathered, positive correlations
respectively). (p < 0.01) are found between concentrations of DOC and MMHgUNF
(r ¼ 0.89), MMHgF (r ¼ 0.76) or %MMHgF (r ¼ 0.65). Thus, the rise of
DOC and salinity (including sulfate) combined with neutral to
3.3. Mercury speciation in surface water of Lakes Titicaca and Uru- alkaline pH along the continuum (from Lago Mayor to Lago Menor
Uru and Lake Uru-uru) support the hypothesis of rising favorable con-
ditions for sulfate-reducing bacteria to produce MMHg (Acha et al.,
Dissolved gaseous Hg (DGM) was low at most locations in both 2017). In parallel, the % MMHg associated to truly dissolved and
investigated lakes and never exceeded 1%THgF. Such DGM levels colloidal fraction (i.e. < 0.22 mm) rose in surface water from Lago
were similar to those found in other great lakes of lower altitude Mayor (43± 33%) to Lago Menor (53 ± 16%) and Lake Uru-Uru
(Table 3) demonstrating that both Titicaca and Uru-Uru lakes have (68± 22%) (S.I.3) together with DOC content suggesting the idea
limited gaseous Hg production in agreement with the low TGM that in this ecosystem organic ligands stabilize dissolved MMHg.
levels measured in the air (Table 1). Although these levels were low, Furthermore, high DOC content in shallow waters are probably
highest concentrations were observed in open waters of Lago more effective to quench UV radiation penetration in surface water
Mayor and Menor suggesting higher Hg photo-reduction to (and thus photo-demethylation) than to enhance photosensitiza-
elemental Hg in open water where DOC content is low (Fig. 2). tion of photochemical pathways. Altogether, these results suggest
Filtered and unfiltered THg levels (THgF and THgNF) in surface an important in situ MMHg production and/or limited degradation
water (Fig. 2) were low in the entire Lake Titicaca and fell in the favoring its accumulation in water of these high altitude endorheic
lowest range of reported concentrations for other great lakes lakes.
worldwide (Table 3) (Mudroch et al., 1988; Meuleman et al., 1995;
Mason and Sullivan, 1997; Campbell et al., 2003a, 2003b; Ramlal
et al., 2003; Rolfhus et al., 2003) illustrating the general pristine 3.4. Mercury levels and biomagnification in food webs
state of Lake Titicaca. However, an increasing trend in concentra-
tions was observed with lowest THgF and THgUNF concentrations Total Hg concentrations increased significantly across the food
measured in the oligotrophic Lago Mayor (IL) and highest webs of the Lago Menor and Lake Uru-Uru illustrating clearly Hg
 S. Gu
edron et al. / Environmental Pollution 231 (2017) 262e270 267

Table 3
Comparison of filtered and unfiltered total mercury (THg), monomethylmercury (MMHg) and dissolved gaseous mercury (DGM) concentrations in Lakes Titicaca and Uru-Uru
with literature data for world's great lakes. Superscripts (a & b) refer to bibliographic reference (right column) from which data originate.

Area Altitude Sampling period THgF THgUNF MMHgF (ng L
1) MMHgUNF DGM (pg L
1) Reference
(m a.s.l) (ng L
1) (ng L
1) (%MMHgF) (ng L
1)
(%MMHgUNF)

Titicaca e Lago Mayor 3809 2013 & 2015 0.11e0.37 0.08e0.49 0.003e0.015 0.013e0.021 7.11e11.2 This study
(1.5 ± 1.1%) (5.4 ± 5.2%)
Titicaca e Lago Menor 3809 2013 & 2015 0.10e0.82 0.18e1.81 0.007e0.243 0.024e0.306 0.78e17.3 This study
(16 ± 13%) (20 ± 12%)
Lake Uru-Uru 3686 2013 & 2015 0.98e2.26 2.06e5.76 0.09e1.03 0.72e1.83 0.05e16.5 This study
(42 ± 17%) (35 ± 6%)
Lake Victoria 1133 1996 to 1998a 3e15.5 a,b
0.064e0.133b Ramlal et al. (2003)a;
Campbell et al. (2003a, 2003b)b
Lake Baïkal 456 1992 & 1993a 0.14e0.77a 0.002e0.038 a
Meuleman et al. (1995)a
Lake Superior 180 2000b 0.44e0.64b 0.004e0.006 b
17e23 b
Mudroch et al. (1989);
Rolfhus et al. (2003)b
Lake Michigan 176 1994 & 1995b,c 0.17e0.55a,b 0.28e0.70b 0.009e0.018b 14e26 c
Mudroch et al. (1988)a;
Mason and Sullivan (1997)b;
Vette et al. (2002)c

biomagnification processes in these high altitude lake ecosystems order or slightly higher than the lowest values reported for other
(Fig. 3). THg levels measured across the food webs in the Lago high altitude pristine regions from central US, Europe and Canada
Menor increased by two orders of magnitude, ranging from and the Tibetan plateau (S.I.5). Hg levels in fish from the Lago
16 ± 3 ng g
1 (dw) in Andean Coot Fulica ardesiaca blood samples to Menor and Lake Uru-Uru are similar to those documented in the
1787 ± 291 ng g
1 in White-Tufted Grebe Rollandia rolland blood Tibetan plateau at locations where moderate Hg contamination is
samples. In the middle of the trophic chain, THg levels were lower suspected (Shao et al., 2016; Zhang et al., 2014). Overall, Hg levels in
in benthopelagic omnivorous fishes (Orestias Spp.; 337 ± 32 ng g
1), the two dominant fish species consumed by the Bolivian and
relative to piscivorous pelagic fishes (O. bonariensis; Peruvian local populations are significantly lower than the
723 ± 268 ng g
1) foraging at a higher trophic level. Overall, THg threshold (500 ng g
1 ww, estimated to 2000 ng g
1, dw, applying a
concentrations in each comparable species and tissue matrix were moisture content of 75%) established by the European Union
significantly higher (p < 0.05) in Lake Uru-Uru relative to the Lago commission (2006). An exception exists for fish collected in the
Menor except for piscivorous pelagic fishes (O. bonariensis) for vicinity of the Ramis river mouth (affected by intense gold mining
which bigger individuals were collected in lake Titicaca activities) where Hg contents are close to the safety limits consid-
(210 ± 20 mm, N ¼ 11) relative to lake Uru-uru (150 ± 30 mm, ered by the European Union commission (EUC, 2006).
N ¼ 11). THg concentrations in lake Uru-uru food webs ranged from
174 ± 45 ng g
1 in Andean Coot Fulica ardesiaca blood samples 3.5. Hg contamination of lakes from the Altiplano: current status
(herbivorous, lowest trophic position) to 2685 ± 755 ng g
1 in and future trends
White-Tufted Grebe Rollandia rolland blood samples (piscivorous,
highest trophic position), respectively. The unique set of results obtained in our study demonstrates
Hg speciation analysis on selected biological samples indicated that major sources of Hg contamination (i.e., urban and mining
that MMHg accounted for 58± 12% of HgT (N ¼ 5) and 26± 16% of effluents), despite their significant amount, have limited dispersion
HgT (N ¼ 21) in zooplankton from lake Uru-Uru, and in the Lago in Lake Titicaca. This can be explained by their retention in the
Menor, respectively. Methylmercury was found to be the dominant coastal areas where the dense cover of totoras traps more than 95%
Hg compound in Orestias Spp. and O. bonariensis muscle tissues, of particle (Pourchet et al., 1994). Furthermore, Hg contamination
accounting for 92± 10% (N ¼ 20), and 94± 6% (N ¼ 20) of HgT due to mining emissions is attenuated at the mouth of Suchez (this
concentrations, respectively in both lakes. study) and Ramis rivers (Gammons et al., 2006) due to the
In situ MMHg baseline production is likely the driver of this Hg remoteness of mining centers. In opposition, Lake Uru-Uru depicts
concentration offset documented among the food webs in both a higher Hg contamination state due to the higher density and vi-
Lakes since higher MMHg levels are reported in both sediment and cinity of urban and mining centers around this shallow ecosystem
surface water of Lake Uru-Uru compared to Lago Menor (Table 2 (Alanoca et al., 2016b).
and Fig. 2). Similarly, the comparison of Hg levels in fish to exist- Despite generally low or moderate THg levels, the specificity of
ing data from the Lago Mayor (S.I.5) revealed that THg contents in the Altiplano Lakes compared to other great lakes is the relatively
Orestias and O. bonariensis fish were respectively approximately 2 high proportion of MMHg in water which reaches up to 50%. As
and 5 times lower in Lago Mayor (Monroy et al., 2014) than those discussed in the previous section, these high MMHg percentages
from the Lago Menor (this study). This relative difference among can be explained by (i) high MMHg production in an environment
Lake Titicaca sub-basins is also consistent with the significantly favorable to methylating micro-organisms (e.g., sulfate rich water
lower MMHg levels measured in surface water samples from Lago and sediment, lower dissolved oxygen levels, neutral to alkaline
Mayor compared to Lago Menor (Fig. 2 and Table 3). However, Hg water, shallow areas etc …), (ii) stabilization and accumulation of
concentrations reported for two fish species (325e1840 ng g
1, MMHg in waters due to abundant (in)organic ligands and (iii) low
S.I.5) at the Ramis river mouth in Lago Mayor (Fig. 1) which is degradation of MMHg in organic rich waters.
largely affected by intense Hg emission due to gold mining activ- The recent eutrophication event in the Lago Menor (April 2015;
ities (Monroy et al., 2014; Gammons et al., 2006) are significantly Acha et al., 2017) which lead to the deoxygenation of water and the
higher (t-test, p < 0.05) than all Hg levels measured in our study. rise of hydrogen sulfide and MMHg in surface water highlighted the
Apart from these point source impacted fish species at the Ramis vulnerability of this ecosystem to anthropogenic pressure. Due to
river mouth, Hg levels in fish from the Lago Mayor are of the same its shallow water column (average 9 m) and rising urban
268 S. Gu
edron et al. / Environmental Pollution 231 (2017) 262e270

Fig. 2. Box plot presentation of dissolved gaseous mercury (DGM), dissolved organic carbon (DOC), total filtered (F) and unfiltered (UNF) mercury and methylmercury in surface
waters (0e1 m) along the upstream e downstream gradient from Lake Titicaca to Uru-Uru. Box plots show the minimum, median (full line), and maximum of each data set (black
point are outlier of the 5th/95th percentiles and N is the number of samples). Data from Uru-Uru Lake are from the campaign sampled at point UU12 during the late wet and dry
season 2014 and 2015. IL: Isla de la Luna, CH: Chua, HU: Huatajata, BC: Cohana Bay, UU: Uru Uru.

development, Lago Menor might be subject to recurrent eutro- heterotrophic or even eutrophic state due to increasing OM and
phication events (Acha et al., 2017) and chemical contaminants nutrients input which may result in enhanced MMHg production
inputs (Duwig et al., 2014) in the upcoming years. For such a sce- and accumulation in the water column and eventually biota
nario, Lake Uru-Uru would be the best current analogue of extreme (Soerensen et al., 2016), and (iii) long lasting anoxic events, as a
eutrophication state. This scenario is less likely in Lago Mayor consequence of recurrent eutrophication events, resulting in
which has a water volume more than 70 times larger than Lago increased H2S concentrations and consequently higher MMHg
Menor. Considering the current trends of growing population and production in the water column (Acha et al., 2017). Although such
urbanization around Lake Titicaca possible Hg pollution scenarii scenarii, tend to favor the hypothesis of a rise in MMHg concen-
could be (i) an increase in Hg inputs (e.g., riverine and atmospheric) trations at the ecosystem scale, the risk for humans has to be
resulting in increasing Hg levels in all environmental compart- moderated since levels remains on or below the EUC, WHO & UNEP
ments likely to Lake Uru-uru, (ii) the shift from oligotrophic to guidelines, mainly due to the short trophic chains (and local
 S. Gu
edron et al. / Environmental Pollution 231 (2017) 262e270 269

Fig. 3. Mean total mercury (THg) concentrations (ng g
1, dw) in key sentinel biological organisms collected in Lake Titicaca (Lago Menor) and Lake Uru-Uru. Error bars represent
one standard deviation and N is the number of samples. THg levels in fish were determined on freeze-dried muscle samples. THg levels in water birds were determined on freeze-
dried whole blood samples. European Commission (EUC, 2006) Hg concentrations guidelines are indicated for comparison.

population diet is not only based on fish consumption). We References

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