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Environmental Science and Pollution
Research
ISSN 0944-1344
Volume 22
Number 13
Environ Sci Pollut Res (2015)
22:10019-10033
DOI 10.1007/s11356-015-4185-4
Early diagenesis and clay mineral
adsorption as driving factors of metal
pollution in sediments: the case of Aveiro
Lagoon (Portugal)
Maria Virgínia Alves Martins, Miguel
Ângelo Mane, Fabrizio Frontalini, José
Francisco Santos, Frederico Sobrinho da
Silva, et al.
1 23
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RESEARCH ARTICLE
Maria Virgínia Alves Martins & Miguel Ângelo Mane &
Fabrizio Frontalini & José Francisco Santos & Frederico Sobrinho da Silva &
Denise Terroso & Paulo Miranda & Rubens Figueira & Lazaro Luiz Mattos Laut &
Cristina Bernardes & João Graciano Mendonça Filho &
Rodolfo Coccioni & João M. Alveirinho Dias & Fernando Rocha
Received: 3 September 2014 /Accepted: 29 January 2015 /Published online: 11 February 2015
#
Springer-Verlag Berlin Heidelberg 2015
Abstract This work aims to define the factors driving the
accumulation of metals in the sediment of the lagoon of
Aveiro (Portugal). The role of initial diagenetic processes in
controlling trace metal retention in surface sediment is traced
by mineralogy, magnetic susceptibility and geochemical anal-
yses. Although several studies have focused on the metal dis-
tribution in this polihaline and anthropized coastal lagoon,
most of them have been solely focused on the total metal
Responsible editor: Céline Guéguen
Electronic supplementary material The online version of this article
(doi:10.1007/s11356-015-4185-4) contains supplementary material,
which is available to authorized users.
M. V. A. Martins
:
M. Â. Mane
Universidade do Estado do Rio de Janeiro, Faculdade de Geologia,
Av. São Francisco Xavier, 524, Maracanã, 20550-013 Rio de
Janeiro, RJ, Brazil
M. Â. Mane
e-mail: miguelmane@yahoo.com
M. V. A. Martins
Universidade do Estado do Amazonas, Av. Djalma Batista, 3578,
Flores, 69050-010 Manaus, Brazil
M. V. A. Martins (*)
:
J. F. Santos
:
D. Terroso
:
P. Miranda
:
F. Rocha
Departamento de Geociências, GeoBioTec, Universidade de Aveiro,
Campus de Santiago, 3810-193 Aveiro, Portugal
e-mail: virginia.martins@ua.pt
J. F. Santos
e-mail: jfsantos@ua.pt
D. Terroso
e-mail: laraterroso@ua.pt
P. Miranda
e-mail: pfnmiranda@gmail.com
F. Rocha
e-mail: tavares.rocha@ua.pt
F. Frontalini
:
R. Coccioni
Dipartimento di Scienze della Terra, Università degli Studi di Urbino
BCarlo Bo^ della Vita e dell’Ambiente (DiSTeVA), Urbino, Italy
F. Frontalini
e-mail: fabrizio.frontalini@uniurb.it
R. Coccioni
e-mail: rodolfo.coccioni@uniurb.it
F. S. da Silva
:
J. G. M. Filho
Laboratório de Palinofácies & Fácies Orgânicas – LAFO,
Universidade Federal do Rio de Janeiro – UFRJ, Av. Athos da
Silveira, 274 (prédio do CCMN), bloco G, Campus Ilha do Fundão,
21., 949-900 Rio de Janeiro, RJ, Brazil
F. S. da Silva
e-mail: fsobrinho@gmail.com
J. G. M. Filho
e-mail: graciano@geologia.ufrj.br
R. Figueira
Instituto Oceanográfico, Universidade de São Paulo, São
Paulo, Brazil
e-mail: rfigueira@usp.br
Environ Sci Pollut Res (2015) 22:10019–10033
DOI 10.1007/s11356-015-4185-4
Early diagenesis and clay mineral adsorption as driving factors
of metal pollution in sediments: the case of Aveiro Lagoon
(Portugal)
Author's personal copy
concentrations. This study instead represents the first attempt
to evaluate in a vast area of the Aveiro Lagoon the role of
biogeochemical processes in metal availability and distribu-
tion in three extracted phases: exchangeable cations adsorbed
by clay and elements co-precipitated with carbonates (S1),
organic matter (S2) and amorphous Mn hydroxides (S3). Ac-
cording to the sediment guideline values, the sediment is pol-
luted by, for instance, As and Hg in the inner area of the
Murtosa Channel, Pb in the Espinheiro Channel, Aveiro City
canals and Aveiro Harbour, and Zn in the northern area of the
Ovar Channel. These sites are located near the source areas of
pollutants and have the highest total available concentrations
in each extracted phase. The total available concentrations of
all toxic metals are however associated, firstly, with the pro-
duction of amorphous Mn hydroxides in most of the areas
and, secondly, with adsorption by organic compounds. The
interplay of the different processes implies that not all of the
sites near pollution sources have polluted surface sediment.
The accumulation of metals depends on not only the pollution
source but also the changing in the redox state of the sedi-
ments that may cause alterations in the sediment retention or
releasing of redox-sensitive metals. Results of this work sug-
gest that the biogeochemical processes may play a significant
role in the increase of the pollutants in the sediment of the
Aveiro Lagoon.
Keywords Metals
.
Speciation
.
Diagenetic processes
.
Mineralogy
.
Aveiro Lagoon
.
Portugal
Introduction
Ria de Aveiro (NW Portugal) is a shallow coastal lagoon with
a surface area of about 45 km
2
. It is formed by several
branches and a complex system of coves, isles and narrow
channels (Fig. 1). The lagoon operates as a multi-estuarine
system, receiving salt water from the Atlantic through an ar-
tificial inlet and freshwater from several small streams, with
catchment areas ranging from 30 to 300 km
2
(Figueiredo da
Silva and Duck 2001). The Vouga and Antuã Rivers, with an
average flow of ca. 50 and 5 m
3
s
−1
, respectively, are the major
sources of freshwater (Moreira et al. 1993;Diasetal.1999).
The region around the lagoon is densely populated and has
experienced a very rapid growth of agriculture, fishery, indus-
trialization, and urbanization since the end of the eighteenth
century. In addition, rapid economic development during the
twentieth century has brought about great pressure and pollu-
tion in this coastal environment (e.g. Pereira et al. 2009 and
references herein; Martins et al. 2010, 2013; Pastorinho et al.
2012). There is evidence that in the most polluted zones asso-
ciated with the rivers and stream runoffs, metals are incorpo-
rated by plankton and transferred through the web chain,
reaching a reas far away from the anthropogenic sources
(Monterroso et al. 2003) and eventually affecting fish (Pereira
et al. 1998a; Abreu et al. 2000; Cid et al. 2001).
Studies aiming to evaluate pollution problems are impor-
tant in this ecosystem as it supports abundant invertebrates,
aquatic birds and fish populations, and allows economic ac-
tivities such as the harvesting of shellfish, aquaculture and
bivalve cultivation for human consumption (AMBIECO
2011).
The far end of the Murtosa Channel is one of the most
studied areas in Ria de Aveiro. The area has experienced the
impact of liquid effluent and waste thrown by the industrial
complex of Estarreja into several streams that connect this
entrance to the main lagoonal body. This zone has thus been
affected by the accumulation of several metals such as Hg and
Cd which are retained in the sediment or reintroduced into the
water column and dispersed by tidal currents (Lucas et al.
1986;Halletal.1987; Pereira et al. 1997, 1998a, b;Abreu
et al. 2000).
Sediment is a matrix of materials comprising detritus, clay
minerals, silicate, and inorganic and organic particles. It is
relatively heterogeneous in terms of its physical, chemical
and biological characteristics (Wu et al. 2011). Sediment also
reproduces the processes occurring in the water column and
can record the changes for longer periods than water. Among
the various contaminants, metals are a major cause for con-
cern, particularly due to their environmental persistence, bio-
geochemical recycling, biological concentration, biological
toxicity, adsorption–desorption, redox, precipitation, solubili-
zation, flocculation, chelation and associated ecological risks.
The degree of sediment pollution is generally estimated by
the analysis of total metal concentrations and comparisons
with suitable reference values. Following this methodology,
Pastorinho et al. (2012) determined the total concentrations of
Cd, Pb, Cr, Cu and Zn in whole-sediment samples collected
from 34 sites in the Ria de Aveiro. These authors determined
several enrichment factors and concluded that the bottom sed-
iment was mostly unpolluted, although Zn was considered to
be a metal of concern in this lagoon.
L. L. M. Laut
Laboratório de Micropaleontologia – LabMicro, Universidade
Federal do Estado do Rio de Janeiro – UNIRIO, Av. Pasteur, 436,
Urca, Rio de Janeiro 22290-240, Brazil
e-mail: lazarolaut@hotmail.com
C. Bernardes
Departamento de Geociências, CESAM, Universidade de Aveiro,
Campus de Santiago, 3810-193 Aveiro, Portugal
e-mail: cbernardes@ua.pt
J. M. A. Dias
CIMA, Centro de investigação Marinha e Ambiental, Universidade
do Algarve, Campus de Gambelas, Faro, Portugal
e-mail: jdias@ualg.pt
10020 Environ Sci Pollut Res (2015) 22:10019–10033
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Total metal concentrations clearly define the total metal
load of sediment, but they do not provide any useful informa-
tion about the biological availability or mobility of the metals
in each polluted area (Räisänen and Hämäläinen 1991). In
fact, within sediment and surface soils, metals occur in several
states of varying mobility, leachability and bio-availability
(Wu et al. 2011).
The differentiation of metal fractions by sequential chemi-
cal extractions allows an assessment of sources, the estimation
of the bioavailability of metal pollutants and the estimation of
the potential remobilization of metals under changing envi-
ronmental conditions (Förstner 1987). Therefore, sequential
extraction provides more complete information that allows
the production of a more detailed characterization of the ori-
gin, chemical form, distribution and potential availability of
metals. Bioavailability, which is the amount of a substance
available or accessible to living organisms, is the most impor-
tant characteristic of contaminant evaluation when dealing
Fig. 1 Study area and sites in Ria
de Aveiro. OC Ovar Channel,
MtC Murtosa Channel, EC
Espinheiro Channel, MC Mira
Channel, AH Aveiro Harbour, BR
Boco River, VR Vouga River, AR
Antuã River, FR Fontela River,
GR Gonde River
Environ Sci Pollut Res (2015) 22:10019–10033 10021
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with environmental issues (Wu et al. 2011). Accordingly, it is
widely accepted that metal effects on biota are related to their
bioavailability, which is in turn mostly dependent on their
chemical forms, rather than on the total concentrations within
the sediment (Förstner 1993). Non-available metal forms are
associated with the crystalline structure of minerals that are
relatively immobile in the long-term, whereas bioavailable
metal forms, due to their mobility in response to any changes
in the physicochemical conditions of terrestrial or aquatic en-
vironments (Förstner 1987), are of concern as they may en-
danger the biosphere.
The first studies aiming to understand the availability of
various metals in Ria de Aveiro were carried out by Martins
et al. (2010, 2015). These authors analysed the effect of the
increasing concentrations of bioavailable metals in benthic
foraminifera. They concluded that mixtures of several bio-
available contaminants are important factors of stress for these
benthic organisms.
This study aims to assess the degree of contamination, dis-
tribution character, pollution status, mobility and availability
of 12 metals (Ag, As, Cd, Cu, Fe, Hg, Mn, Ni, Pb, Sb, Sn and
Zn) in the Aveiro Lagoon (Portugal). The mobility and avail-
ability of these metals in 53 surficial sediments are examined
using a three-stage sequential chemical extraction technique.
It also addresses the relationship among these metals and the
possible occurrence of initial diagenetic processes associated
with organic matter degradation.
Materials and methods
This study integrates textural, physico-chemical, geochemical
and mineralogical data from 53 surface sediment samples col-
lected in July 2011 from sites located in intertidal and tidal
flats areas surrounding the main channels of Ria de Aveiro
(Fig. 1; Appendix 1). Part of these data were previously
analysed by Martins et al. (2015) to evaluate the pollution
effect on benthic foraminifera. Methodology used in the ac-
quisition of sediment grain size and geochemical and miner-
alogical data is reported also in Martins et al. (2015). This
work is however based on a wide and more detailed charac-
terization of the mineralogical composition of the sediments
incl uding the analys is of the fr actions <63 μm(fine)and
<2 μm (clay) by applying X-ray diffraction (XRD) tech-
niques. The methodology described by Martins et al. (2007)
for i dentification and semiquantification of minerals was
adopted. The degree of the structural order–disorder of the
minerals was carried out on diffractograms of assemblies in
the natural state using the Kubler (1964) and Segonzac (1969)
index of the crystallinity of illite, which is based on measuring
the width (in 2Θ) of the half-height of reflection (001) at 10 Å.
Higher values of this index are indicative of the lower crystal-
linity of illite.
The magnetic susceptibility (χ) of the sediment was mea-
sured in the fine fraction with a portable KT-9 Digital Mag-
netic Susceptibility Meter by taking ten successive readings
per sample and using the mean values obtained . Textural,
mineralogical, magnetic susceptibility and some physico-
chemical parameters (pH, Eh, measured in surface sediments)
were also used to understand the distribution of total organic
carbon (TOC) and the total elemental co ncent rations an d
chemical fractionation of metals (Ag, As, Cd, Cu, Fe, Mn,
Ni, Pb, S, Sb, Sn and Zn). The available concentrations of
these chemical elements (except S), as well as of Hg, were
evaluated in the following phases: S1, elements concentra-
tions of exchangeable cations adsorbed by clay and elements
co-precipitated with carbonates; S2, elements concentrations
adsorbed by organic matter; and S3, elements concentrations
adsorbed by amor phous Mn hydroxides. In this work, the
distribution of metal’s (Me) available concentrations in each
extracted phase (Me-S1, Me-S2, Me-S3) was analysed. Each
metal’s residual phase (Me-R) (almost corresponding to ele-
mental concentrations retained in the mineralogical crystalline
structure) was also calculated by the difference between total
concentrations (Me-T) and total available concentrations (Me-
TA): (Me-T)–(Me-TA)). Moreover, the percentage of avail-
able concentrations for each metal (Me-%TA) relative to the
residual phase (Me-R) was also evaluated.
Data analysis
The analysed data was logarithmically transformed log(1+X)
before the statistical analysis. The cluster analysis (CA) in the
R-mode and Q-mode was based on the ‘complete linkage’
method for agglomeration and the 1-Pearson r correlations,
with the aim being to group the variables and stations, respec-
tively, with similar patterns of distribution. A matrix of Pear-
son correlations was also determined to investigate the rela-
tionship between variables (with a significance level p<0.05).
Pearson correlations and the CA were carried out in Statistica
8.0. Maps were produced with ArcGis 9.2®. The metric coor-
dinates used are according to the WGS84 (UTM 29) datum.
Results
The maximum, minimum and mean values of the variables
analysed in this work are presented in Appendix 1,whereas
the matrix of correlation is presented in Appendix 2.The
sediment mean grain size (SMGS) values (Fig. 2), which var-
ied between 18.4 and 368 μm (mean 85.4 μm),revealthatthe
sediments are mostly composed of muddy sand or sandy mud
in the studied sites (except in station 7). The variability of the
SMGS values is mostly dependent on the sand fraction con-
tent and in particular with the 63–125-, 125–250-, 250–500-
and 500–1000-μm fraction contents according to the
10022 Environ Sci Pollut Res (2015) 22:10019–10033
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significant positive correlations (Appendix 2). The values of
sorting vary between 1.5 and 5.7 (mean 0.89), which indicates
that the sediment is poorly to extremely sorted. Sorting is
significant and negatively correlated with the SMGS and, pos-
itively, with the sediment fine fraction and TOC (Appendix 2).
The TOC content varying from 0.1 to 7.4 % (mean 2 %) is
significantly and positively correlated with the fine fraction,
phyllosilicates and pyrite, and negatively with the SMGS and
the coarser sand fraction content (125–250, 250–500 and
500–1000 μm; Appendix 2).
The magnetic susceptibility values are negative, ranging
from −0.10 to −0.38 SI unities (Fig. 2). This parameter has
significant positive correlations with the fine sand fraction
(125–250 μm), fine fraction (<63 μm) and sorting but has
no significant correlation with the mineralogical data
(Appendix 2).
A conventional XRD analysis indicates that the sedi-
ment is mostly composed of phyllosilicates (22–68 %;
mean 44 %), quartz (15–44 %; mean 31 %) and feldspars
(4–37 %; mean 10 %), with several accessory minerals,
namely calcite (<7 %; mean 1 % ), siderite (<5 %; mean
1 %), pyrite (0.6–5 %; mean 2 %) and minor occurrences
of anhydrite (<5 %; mean 2 %), anatase (<4 %; mean
1%),dolomite(<3%;mean0.5%),magnesite/
maghemite (<2 %; mean 0.3 %) and jarosites (<2 %;
mean 0.1 %). Although magnetite (Fe
3
O
4
) can be found
in many igneous and metamorphic rocks, which are the
most common lithologies in the hydrographical basins of
the rivers flowing into the lagoon, the mineral is not de-
tected by the XRD analysis in the studied sediment. Rel-
atively high values of phyllosilicates and K -feldspars are
more common in internal lagoonal areas (Fig. 2).
Significant positive correlations are observed between fine
fraction, sorting, TOC, phyllosilicates and pyrite content (Ap-
pendix 2). The phyllosilicates (Fig. 2) are negatively correlat-
ed with quartz, plagioclase and K-feldspars (Appendix 2). Py-
rite is also significantly and positively correlated with siderite;
both variables are negatively correlated with SMGS and
(Appendix 2).
The clay fraction of the studied sediment is character-
ized by a quite similar clay mineral assemblage (Appen-
dix 1) composed mostly of il lite (51–85 %; mean 72 %),
kaolinite (11–49 %; mean 25 %), chlorite (<11 %; mean
1 %), smecti te (<3 %; mean 0.3 % ) and vermiculite
(<8 %; mean 2 %). Illite occurs commonly in higher per-
centages in the clay fraction near the mouths of the rivers,
located in internal lagoonal zones, decreasing towards the
lagoon mouth (Fig. 2). Illite is significantly and
Fig. 2 Maps of distribution of sediment mean grain size (SMGS; μm), magnetic susceptibility (Mag. S.), phyllosilicates (Phy;%),K-feldspars(K-Felds;
%), illite (Ill; %) and Kubler Index (KI). Legend as in Fig. 1
Environ Sci Pollut Res (2015) 22:10019–10033 10023
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negatively correlated with kaolinite content, sand fraction
and magnetic susceptibility (Appendix 2). The distr ibu-
tion of vermiculite and smectite documents the fact that
relatively high values of these minerals occur more fre-
quently in the inner lagoonal area connected with the river
fluxes. The Kubler index (from 0.2 to 0.7; mean 0.4)
reaches relatively high values near the lagoon entrance
(Fig. 2) that is indicative of the lower crystallinity of illite.
The distribution of total concentrations of Ag, As, Cd, Cu,
Fe, Mn, Ni, Pb, S, Sb, Sn and Zn (evaluated by the total
digestion of sediments) shows large elemental variations in
the study area (SM Fig. 1). Some elements are significant
and positively correlated (Appendix 2) with TOC, such as
Cu, Fe, Ni, S, Sb, Sn and Zn, with fine fraction such as Ni,
S, Sb and Sn, with phyllosilicates such as Fe, Ni and Sn, with
pyrite, such as Fe, Ni, S, Sn and Zn, and with siderite, such as
Fe, Mn and Ni. Total concentrations of these elements gener-
ally co-vary with the respective TA (Me-TA=S1+S2+S3)
according to the significant and positive correlations among
them (Appendix 2). Thus, distributions of TA of metals
(Fig. 3;SMFig.2) show increased values in the same areas
where total metal c oncentrations increase. However, the
ranges of percen tages of total available concen trations
(Me-%TA; Appendix 1) evidence that for those metals that
reach the highest availability, such as Zn (5–99 %; mean
71 %), Pb (18–99 %; mean 58 %), Cd (2– 96 %; mean
57 %), Ag (1–77 %; mean 9 %), As (15–60 %: mean 46 %)
and Cu (8–50 %; mean 26 %), the values are highly variable.
Considering the d ifferen t extract ed phase s of met als,
the highest available c oncentrations (Me-S1, Me-S2, Me-
S3) of As, Cd, Fe, Ni, Mn, Pb and Zn are commonly
associated with the S3 phase and of Ag, Cu and Sn are
mostly linked with the S2 phase (SM Fig. 4). The maps of
distribution and biplots of each metal’s available concen-
trations evidence the relative importance of each sediment
phase and discriminates lagoonal areas in terms of their
availability (SM Figs. 3 and 4).
Relationships among the sedimentological
and physicochemical data
The R-mode cluster analysis (CA) was carried out to identify
similar patterns of distribution between Me-TA and the other
sedimentological and physicochemical data (Fig. 4). The re-
sults show that most of the Me-TA (except for Pb, Sb and Sn)
are related to fine- grained se diment enriched in TOC and
phyllosilicates and tend to increase with the rise of sorting
and pH. This kind of sediment is also characterized by
Fig. 3 Maps of distribution of total available concentrations (TA) of As, Cu, Fe, Mn, Pb, Zn, Hg and Sn. Legend as in Fig. 1
10024 Environ Sci Pollut Res (2015) 22:10019–10033
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relatively high siderite and pyrite contents and magnetic sus-
ceptibility values. Total available concentrations of Pb, Sb and
Sn ar e more related to coarser sediments (as revealed by
granulometric and mineralogical data) and more oxic sedi-
ments (high Eh values).
The Q- mode CA, based on available concentrations of
metals (Ag, As, Cd, Cu, Fe, Hg, Mn, Ni, Pb, Sb, Sn and Zn)
in S1, S2 and S3, allows the recognition of five groups of
stations (Figs. 5 and 6).Themeanvaluesofallthevariables
were calculated to facilitate the identification of differences
among these groups (Appendix 3).
Group 1 includes sites, located in Murtosa Channel and in
the northern extremity of Ovar Channel; these stations are
characterized by fine-grained sediments with the highest con-
centrations of Hg in S2 and Mn-TA (with significant concen-
trations in all phases) and pyrite, low Eh values and relatively
high TOC, phyllosilicates (namely kaolinite) and Fe-TA con-
tent. Group 2 comprises sites placed in the northern and
Pb-TA
Dol
Zirc
Calc
Alun
Flds K
Qtz
Magn
Jar
Anhy
Sn-TA
Sb-TA
Opal
Plag
Zeol
SMGS
Eh
Hg-TA
Cu-TA
Ag-TA
Ni-TA
As-TA
MagS
Phy
TOC
FineF
Sort
Anat
Pyr
Sid
Zn-TA
Cd-TA
Mn-TA
Fe-TA
pH
0,0
0,5
1,0
1,5
2,0
Linkage Distance
Fig. 4 R-mode cluster analysis
applied to identify similar patterns
of distribution in selected textural,
mineralogical and geochemical
data. It compares total available
concentrations (TA) of metals
with the other variables
48
44
43
49
47
41
42
40
39
52
51
50
38
37
35
34
36
33
32
31
7
9
6
5
53
12
11
17
4
30
28
25
29
46
45
23
26
22
16
10
15
8
14
13
3
2
24
20
21
19
18
27
1
0,00
0,02
0,04
0,06
0,08
0,10
0,12
Linkage Distance
1.2.3.4.5.6.
Fig. 5 Q-mode cluster analysis
based on available concentrations
of metals in S1, S2 and S3 to
identify groups of sites with
similar characteristics in metal
content
Environ Sci Pollut Res (2015) 22:10019–10033 10025
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eastern sector of the Ria de Aveiro, with the highest concen-
trations of As, C d, Fe, Mn, Ni and Zn, in S3 and higher
concentrations of As, Cd, Fe, Mn and Zn, in S1 and S2. Group
3 includes only the station 7, located in a hydrodynamic area
of Murtosa Channel, with the coarsest sediments and the low-
est values of magnetic susceptibility, TOC and metals, except
for Hg in S2; the highest Eh value is found in this station.
Stations of group 4 are located in the central area of the lagoon
and in the Mira Channel and are characterized by muddy sand
sediments with low magnetic susceptibility, relatively high
values of Eh and concentrations of phyllosilicates (namely
kaolinite), Fe, Mn, Ni and Pb, in S3. Stations of group 5 are
situated in Aveiro harbour area, near the lagoon mouth, and
also include and an anchorage of Aveiro City (Botirões Piers);
in these sites, the sediments are low oxic and have the highest
concentrations of Pb-TA (in S1, S2 and S3) and Sn in S2 and
relatively high Zn-TA, associated with S3. Station 48 located
in Aveiro City (Alboi Canal) represents group 6; it is charac-
terized by very fine sediments with the highest content in
TOC, phyllosilicates (namely illite) and metals such as Cd-
TA, Sb and Zn, in S1 and S2 and Cu, Pb and Sn in S2, and it
has low pyrite content and relatively low pH values.
Discussion
Sedimentary processes and metal retention/mobilization
Using both cluster analysis (Fig. 4) and the correlation
matrix (Appendix 2), the depe ndence of most o f the
Fig. 6 Groups of stations defined
by Q-mode cluster analysis based
on available concentrations of
metals in S1, S2 and S3 (Fig. 5).
Legend as in Fig. 1
10026 Environ Sci Pollut Res (2015) 22:10019–10033
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variables on sediment grain size and other textural fea-
tures is put into evidence. These results indicate that the
lagoon’s hydrodynamics, which are dominated by tidal
forcing (Dias et al. 1999), influence the sediments grain
size and their mineralogical and geochemical composi-
tion. Under low current velocities, fine-grained sediments
(mostly silt and clay) with high proportions of organic
matter are deposited (Lopes and Dias 2007). Rivers intro-
duce in the lagoon mainly fine sediments, since coarse
particles are prevalently deposited in the upstream or at
their mouths. Once in the lagoon, fine-grained sediments
are mainly transported by tidal currents. The suspended
sediment concentr ations in the lagoon are, i n gener al,
much higher during the spring tide and winter (the rainy
season) due to the higher intensity of the currents giving
place to high turbid zones in those areas, induced by
strong tidal currents, tidal asymmetries and river’srunoff
(Lopes et al. 2006). The most important areas of the la-
goon, from the point of view of hydrodynamics and sed-
iments transport, are the S. Jacinto and the Espinheiro
Channels as well as some zones of Murtosa Channel,
which are the most affected by the ocean as well as by
the two major lagoon freshwater contributors, the Vouga
and the Antuã Rivers (Lopes et al. 2006).
The effects of sediment transport through the lagoon be-
come apparent in the maps of the distribution of
phyllosilicates, K-feldspars, illite and the Kubler index values
(Fig. 2). Downstream, the phyllosilicates, K-feldspars and il-
lite content tends to decrease, while the Kubler index values
rise. These results evidence physical degradation of illite and
K-feldspars caused by sedimentary dynamics processes and
probably by that cycles of deposi tion and resuspension of
sediment.
The sedimentary dynamics are mirrored by magnetic sus-
ceptibility values that are mainly dependent on its iron oxide
content, which is dominated by the magnetite and hematite
components that are rare minerals in the studied sediments
since they were not detected by XRD techniques. Minerals
that do not contain Fe (e.g. quartz, halite and calcite) and
organic matter are named diamagnetic and exhibit a negative
magnetization in the presence of a weak magnetic field. The
values obtained for the bulk magnetic susceptibility in the
studied sediments are negative and are therefore in accordance
with the abundance of diamagnetic materials and the scarcity
of magnetic minerals.
The significant positive correlation observed between mag-
netic susceptibility and the fine sand fraction, fines and sorting
means that relatively high magnetic susceptibility values are
due to the contribution of small particles of magnetic Fe-oxide
probably related to inclusions within the framework of small
clastic grains in sediment (Hounslow and Morton 2004), since
coarse sediments are dominated by quartz and feldspars grains
in this area.
Coarse detrital minerals, such as quartz and plagioclase,
increase in areas under the stronger hydrodynamic conditions
near the lagoon entrance (Martins et al. 2014). These zones are
dominated by effective erosion due to intense currents which
induce high bottom stress, whereas the remaining areas of the
lagoon are characterized by net deposition (Lopes and Dias
2007).
In shallow and tidal flat zones, which are characterized by
very irregular geometry contributing to a strong damping of
the currents and an increase of the phase delay of the tidal
wave, fine-grained sediments are deposited and accumulated
(Lopes and Dias 2007). With fine-grained sediments, high
organic matter content (as revealed by significant positive
correlation between TOC and fine fraction) is also
accumulated.
In confined areas located near the river’smouth,theTOC
values are on overall higher due to the contribution of organic
and inorganic nutrients with continental origin. However, ma-
jor transformations in the pools of organic and inorganic nu-
trients that reach the lagoon are related to biological processes
associated with bacteria-plankton (Cunha et al. 2003a, b).
Weather conditions may also influence the biological produc-
tion (Almeida et al. 2005) and accumulation of organic matter,
as well as the coverage by microalgae and seagrass on inter-
tidal areas. This contributes to the accumulation of fine sedi-
ment particles (silt and clay) and organic matter (Figueiredo
da Silva et al. 2009).
In organic-rich sediment, intense bacterial heterotrophic
activity occurs (Hoppe et al. 1996; Cunha et al. 1999, 2000).
Bacteria are important biological components involved in the
turnover (transformation and mineralization) of organic matter
in Ria de Aveiro (Cunha et al. 1999, 2000, 2003a, b). In salt
marsh sediment, bacterial productivities are high and strongly
influenced by the dissolved organic matter (DOM) that is re-
leased after the decomposition of higher plants or exudation
from primary producers (Moriarty and Pollard 1981). The
DOM is readily assimilated and incorporated into the bacterial
biomass or is rapid ly transformed into CO
2
(Creach et al.
1999) with oxygen consumption. The oxygen balance de-
pends on the degradation of organic carbon compounds, deg-
radation of nitrogen compounds (organic nitrogen, ammonia,
nitrite and nitrate), photosynthesis (algae growth/respiration),
bed respiration/re-suspension of organic sediments and re-
aeration processes (Lopes et al. 2008).
In those areas where the degradation of organic m atter
leads to low oxic or anoxic conditions, pyrite can be generated
as a result of microbial activity. Pyrite is identified in our
samples by an XRD analysis, but it can also be observed in
the sediment using a microscope. Framboidal pyrite, which
occurs as infillings and pseudomorphs of the chambers of
foraminiferal tests and frequently as irregularly shaped grains,
is common. Foraminifera provide open spaces for coloniza-
tion and local nutrients for bacterial growth, whereas the cell
Environ Sci Pollut Res (2015) 22:10019–10033 10027
Author's personal copy
walls of the bacteria may provide a local nucleation site for
sulphides (Kohn et al. 1998; Saunders et al. 1997; Frontalini
et al. 2009). The occurrence of framboidal pyrite in the surface
sediment is also a common feature that suggests authigenic
precipitation and indicates intense activity by sulphate-
reducing bac teria near the top of th e sedime nt. M any
sulphate-reducing bacteria produce intracellular ferrimagnetic
greigite (Bazylinski and Moskowitz 1997) that may also con-
tribute to the slight increase in the magnetic susceptibility
values in some areas. It should be noted that several sulphates,
such as anhydrite (CaSO
4
), alunite (KAl
3
(SO
4
)
2
(OH)
6
) and
jarosite (KFe
3
+3(OH)
6
(SO
4
)
2
), are identified in the studied
samples. Pyrite is easily formed and well-preserved in anoxic
environments. The good connection between the Aveiro La-
goon and the sea and the circulation pattern inside the lagoon
are, therefore, responsible for the relatively high level of oxy-
gen content in the water column throughout the main lagoonal
body (Lopes and Silva 2006). However, at the far end of the
lagoon, where the intertidal salt marshes are important, the
dissolved oxygen concentration frequently generates
hypoxic/anoxic conditions (Lopes et al. 2005; Lopes and Silva
2006). In this kind of shallow area, dense populations of bac-
teria and high heterotrophic activity rates occur (Cunha et al.
2000, 2003a, b) that might promote the formation of early
diagenetic minerals. If sulphate is present, it can be used by
sulphate-reducing bacteria and converted into sulphide, while
iron-reducing bacteria can reduce insoluble iron(III) to soluble
iron(II) (Canfield et al. 1993).
The relatively high oxygen concentrations close to the
sea and throughout the main channels may cause pyrite
destabilization in these areas. The oxidation of pyrite
forms sulphuric acid and carbonic acid, which may in turn
lead to a drop in pH values within the sediment. The
degradation of organic matter ma y also pro duce acids
(Leenheer 2007) and contribute to a pH decrease. How-
ever, in the northern area of the Ovar Channel, relatively
high pH values, as well as high pyrite and TOC content,
are observed. These relatively high pH values may be a
conseq ue nc e of the d is ch arge of d om est ic effluent in this
area. In fact, materials added to water during domestic
use, such as detergents and s oap-based products, are often
alkaline and, consequently, may increase the pH of water
and pore water of surface sediments.
Pyrite has significant positive correlations with TOC, sid-
erite and total concentrations of several metals such as Fe, Mn,
Ni, S, Sn and Zn, and TA of Mn and Zn. The significant
positive correlation between pyrite and siderite suggests that
the latter should also be formed b y iron-reducing bacteria
(Coleman 1993; Coleman and Raiswell 1993). Siderite is an
authigenic mineral in sedimentary rocks (e.g. Mozley and
Carothers 1992) that precipitates within the pore spaces of
sediment after deposition (Curtis et al. 1986). Its formation
process depends on pore-water chemical compositions and
microbial activity (Mozley 1989). Experimental studies by
Mortimer and Coleman (1997) have confirmed the crucial role
of Fe-reducing bacteria in the formation process of authigenic
siderite. A consequence of this process might be the pH in-
crease that also fits the values found in the areas with the
highest siderite and pyrite contents.
Methane (CH
4
) release from bottom sediments is a quite
common phenomenon in Ria de Aveiro. Methane is generated
during early diagenesis. Both siderite precipitation and meth-
ane accumulation require interstitial pore waters that have suf-
ficient hig h bicarbonate activities and are depleted in dis-
solved sulphur and free oxygen (Gautier 2006). In slowly
accumulating sediment, most organic matter is probably con-
sumed by aerobic organisms, while sulphate-reducing anaer-
obic bacteria contribute to pyrite formation. However, meth-
ane is generated in areas where there is a more rapid deposi-
tion of large quantities of organic matter (Gautier 2006).
Changes in the redox state of the sediment as a result of
organic matter degradation may influence the concentrations
of redox-sensitive elements, such as Fe and Mn. Both elements
have similar patterns of distribution (as indicated by significant
positive correlation between each other). Sedimentary pore-
water chemistry strongly influences the precipitation and disso-
lution of the Fe and Mn solid phases (Dixon and Skinner 1992;
Schwertmann and Fitzpatrick 1992;StummandMorgan1996;
Drever 1997). Aqueous Fe(II) and Mn(II) are significant in
naturalwatersonlyintheabsenceofO
2
. Insoluble Fe(III) and
Mn(III/IV) oxides form under oxic conditions. In most of the
studied sites, anoxic conditions occur some millimetres below
the surface, as testified by the identification of pyrite in the
surface sediment in most of the studied sites.
According to Rey et al. (2005), magnetic susceptibility can
also reveal the diagenetic remobilization/enrichment of sedi-
ment in redox-sensitive metallic elements like Fe or Mn. Mag-
netic susceptibility has also significant negative correlation
with Mn and positive with As-TA and Cd-TA. These results
suggest that early diagenetic processes may have played a
significant role in the retention or remobilization of metals in
the sediment of Ria de Aveiro.
According to the reference values shown in Table 1,the
studied sites can be considered as non-polluted by Ag, Cd, Cu,
Fe, Mn, Ni and Sb. In contrast, the sediment is polluted by
other elements in some places, for instance, by As and Hg in
the inner area of the Murtosa Channel, by Pb in the Espinheiro
Channel, Aveiro City canals and Aveiro Harbour, and by Zn in
the northern area of the Ovar Channel, the inner zone of the
Murtosa Channel, the Aveiro City canals and Aveiro Harbour,
and the dispersed sites of the Espinheiro Channel. Taking into
account the concentrations indicated by ISQG/TEL and PEL
(Table 1), some issues must be highlighted. Zinc is the main
pollutant in the Aveiro Lagoon. This metal is mainly related to
industrial activities and is supplied by the flow of the rivers, as
inferred by the distribution maps of the Zn-S1, Zn-S2 and Zn-
10028 Environ Sci Pollut Res (2015) 22:10019–10033
Author's personal copy
S3 concentrations (SM Fig. 2). They therefore sometimes ex-
ceed the PEL values, as recorded by S3 at the northern area of
the Ovar Channel or by TA not only in that zone but also in the
Aveiro City canals. For As, TA and the S3 concentrations are
between the ISQG/TEL and PEL levels in the Murtosa Chan-
nel, where they exceed the PEL values. A similar situation is
observed for TA and S2 with respect to the Hg concentrations.
For Pb, TA and the S3 concentrations are between the ISQG/
TEL and TEL values along the Espinheiro Channel, in the
Aveiro City canals and Aveiro Harbour. For Cd, TA is be-
tween the ISQG/TEL and PEL values in the northern area of
the Ovar Channel (and also in some sites in S3), the Murtosa
Channel, the Aveiro City canals and Aveiro Harbour.
Factors influencing the level of pollutants in different zones
of Aveiro Lagoon
The stations of group 2 (Figs. 5 and 6), located in the northern
area of the Ovar Channel and the inner zone of Murtosa Chan-
nel and three harbour areas, are the most polluted by As, Cd,
Fe, Mn, Ni and Zn. In the inner zone of the Murtosa Channel,
the TA concentrations of As, Cd, Cu, Hg, Pb and Zn reach
levels between the ISQG/TEL and PEL in some sites. In this
group of stations, available concentrations of these metals are
mostly associated with organic matter compounds (S2) and
Mn hydroxides (S3). The northern area of the Ovar Channel
and the inner zone of Murtosa Channel (group 2; Figs. 5 and
6) have the contribution of several rivers and streams crossing
industrialized areas. One of the most polluted unit was a chlor-
alkali plant in the industrial complex of Estarreja (Lucas et al.
1986;Halletal.1987; Pereira et al. 1997, 1998a, b;Abreu
et al. 2000). This plant introduced a huge amount of pollutants
including Hg in Aveiro Lagoon through the inner zone of the
Murtosa Channel (Fig. 2). This plant has changed its
labouring process and is not causing pollution as in the past.
In spite of this, the present sediments are yet recording the past
activity of this plant (Pereira et al. 2009). In the stations of
group 2 (Figs. 5 and 6), the sediments are poorly oxygenated
and have high pyrite content and relatively high pH values.
The occurrence of relatively high concentrations of metals
associated with organic matter, high pyrite content and Mn
hydroxides suggests that the active biogeochemical activity
may lead to metals retention. Pyrite formation in anoxic layers
may contribute to metals retention and the precipitation of Mn
hydroxides on oxic surface sediment too. Moreover, Fe and
Mn oxyhydroxides are well-known scavengers for metals
(Benjamin et al. 1996;Nelsonetal.1999), particularly if they
are biogenically derived.
Stations of group 1 include sites located in Murtosa Chan-
nel and in the northern extremity of Ovar Channel with the
highest concentrations of Hg in S2 and Mn-TA (in all phases)
and relatively high concentrations of Fe-TA. These sediments
have also low oxic conditions and are rich in TOC, pyrite and
phyllosilicates (namely clay minerals). Station 7 (group 3;
Figs. 5 and 6), located in the middle zone of Ovar Channel,
has also significant concentration of Hg in S2. The sediment
from other zones of the lagoon has low mercury concentra-
tions (Fig. 2).
The complex geometry of the lagoon seems to limit the
advective transport in the lagoon (Lopes et al. 2001). However,
Table 1 Summary of saltwater sediment concentrations in uncontaminated sediments and guidelines adopted by the Netherlands, Australia and New
Zealand, and Canada
Elements Non-contaminated sediments Sediment quality objectives in the Netherlands Recommended sediment
quality guidelines
(ANZECC/ARMCANZ 2000)
Canadian Council
of Ministers of the
Environment 2002
Background values
(Salomons and Forstner 1984)
Target value Maximum permissible
concentration
Target value ISQG-high ISQG/TEL PEL
mg/kg dry weight
Antimonium 225
Arsenic 29 55 20 70 7.24 41.6
Cadmium 0.17 0.8 12 1.5 10 0.7 4.2
Copper 45 36 73 65 270 18.3 108
Iron 47,000
Lead 20 85 530 50 220 30.2 112
Manganese 850
Mercury 0.3 10 0.15 1 0.13 0.7
Nickel 68 21 52
Silver 13.7
Zinc 95 140 620 200 410 124 271
From ANZECC/ARMCANZ 2000 and from Grimwood and Dixon 1997
Environ Sci Pollut Res (2015) 22:10019–10033 10029
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the location and type of contamination of the stations belonging
to groups 1, 2 and 3 support the idea that the contaminants can
be remobilized, for instance, from the inner zone of Murtosa
Channel and exported to other areas, by currents, adsorbed in
suspended particles, such as clay minerals and organic com-
pounds. During spring tides, approximately 75 % of the water
of the inner zone of the Murtosa Channel is renewed, implying
the export of anthropogenic material previously discharged
there (Hall et al. 1987). In overall, the alternating process of
erosion and deposition associated with very shallow areas and
strong currents activity mostly during spring tides may contrib-
ute to the remobilization and dispersion of pollutants. This phe-
nomenon is also documented by the distribution of illite content
and by the Kubler index values. Part of the accumulation of
pollutants in the Ovar Channel may therefore be related to an
effect of retention, since this part represents one of the most
confined lagoonal zone. This effect would also be favoured
by diagenetic processes.
Stations of group 4 (Figs. 5 and 6) are located in the central
area of the lagoon, including the Espinheiro Channel, several
small channels flanked by tidal flats, the connection with the
Vouga River, and in the southern part of Mira Channel. Oxy-
genated muddy sands with high concentrations of Pb in S3
compose the substrate of these stations. Sediments of this
group have not the highest concentrations of metals, but most
of the metals have their highest concentrations in S3. In both
zones, the shipping traffic is intense that seems to be an im-
portant source of pollution. The central area of the lagoon is
also under the influence of the Vouga River, with several in-
dustries settled in its margins, namely the Cacia pulp mill
factory. The supply of pollutants from this river to the la-
goon may hav e been much higher in the past, before the
construction of the effluent treatment system in the region.
The sedimentary phenomena t hat cause Pb and metals en-
richment in this group of stations may therefore be rather
different from the processes operating in other sectors of the
lagoon. At the Espinheiro Channel, for instance, the Pb con-
centrations decrease from S3 to S1 and to S2. These results
suggest that the Pb and other metals in this group of stations
are mostly associated with inorganic ligands as opposed to
organic matter. Metal adsorption by Mn hydroxides is sig-
nificantly greater than in organic materials, probably
favoured by the abundance of benthic algae on t he sedi-
ment, namely diatoms as suggested by the relatively high
abundance of opal C/T. The production of oxygen by pho-
tosynthesis of these organisms favours the precipitation of
Mn (which is dissolved in anoxic sedimentary pore waters),
on oxic superficial sediment layers.
The sediments of the stations of group 5 (Figs. 5 and 6),
located in protected areas of the Aveiro Harbour in the en-
trance Espinheiro Channel, close to the lagoon mouth, and
of an anchorage of Aveiro City (Botirões Piers) are low oxic
and have the highest concentrations of Pb-TA (in S1, S2 but
especially in S3) and Sn in S2 and relatively high Zn-TA,
associated mostly with S3. Pyrite is present, but TOC and total
available concentrations of Fe and Mn are not as high as in
other zones. Water circulation in these areas is restricted, fa-
cilitating the accumulation of fine-grained sediment and metal
retention. Metal accumulation in this group of stations is re-
lated to harbouring activities and the release of fossil fuels by
ships and boats. The association of Sn and organic matter in
these stations suggests a link between the slight enrichment of
this metal and the pollution caused by tributyltin oxide, which
has been extensively used as antifouling paints for wood pres-
ervation due to its biocide effect. Our data agree with earlier
findings with respect to the role of metal oxides in controlling
metal adsorption. They are also consistent with the results
concerning selective extractions obtained in other studies,
which indicate that Pb is associated predominantly with the
Fe/Mn oxyhydroxide phases of the sediment (Nelson et al.
1999 and references herein). It is possible that Pb could be
co-precipitated during the in situ formation of Mn hydrox-
ide, which could lead to even greater Pb binding by Mn
oxyhydroxides, as also described by Nelson et al. (1999).
The same trend is observed for As, Ni, Cd and Zn, whereas
other metals, such as Cu, Sn, Hg and Ag, are more related
to organic materials in the Aveiro Lagoon. A lterations i n
pH may also influence the relative roles of adsorbing
phases. An increased pH would, for instance, favour the
ionization of carboxyl functional groups on organic mate-
rials and surface hydroxyl groups on oxides (Nelson et al.
1999).
Industrial area of Aveiro City (located in Alboi Canal) is
represented by station 48 (group 6; Figs. 5 and 6). In this
zone, the sedime nts are very fine with low pyrite conte nt
and low pH but with the highest TOC and phyllosilicates
(namely illite) content and relatively high total concentra-
tions of Cu, Pb, Sb, Sn and Zn (Fig. 3;SMFig.4). In
contrast, the contents of Fe and Mn are relatively low.
The relatively low pyrite content may be explained by its
low preservation in low pH sediments. It should be noted
the occurrence of highest available concentrations of
metals, namely of Zn, Cu and Sn, in S1 and S2, and Pb,
in S1. This is a confined area, because the current activity
is weak and limited by several canal locks, which princi-
pally prevent the water movement and its interchange with
the large lagoonal body (Martins et al. 2010). Due to the
minor exchange with the main lagoonal body, the influence
of the material coming from upstream is relatively impor-
tant. This area receives sediment with a large proportion of
phyllosilicates, which are mainly transported in suspen-
sion. The higher concentrations of these elements in this
station (Alboi Canal) may be related to a m etallurgic fac-
tory labouring during the twentieth century (Martins et al.
2010). The a bundance of clay minerals and organic matter
may justify the association of metals with these materials.
10030 Environ Sci Pollut Res (2015) 22:10019–10033
Author's personal copy
Final considerations
The results of this work show that, near the main source areas
of the sediment, there are both low and relatively highly pol-
luted sites. The sediment of the most hydrodynamical areas is,
in general, not or low polluted in the Aveiro Lagoon. Active
tidal currents and water renovation dilute and disperse the
pollutants. Pollutants are accumulated in confined areas where
the sediment is fine and rich in organic matter. In these areas,
the presence of clay minerals and organic matter contributes to
the adsorption of metals. However, the most important phe-
nomena in metal retention seem to be the biogeochemical
processes that are directly or indirectly related, for instance,
to the production of pyrite and the precipitation of Fe and Mn
oxyhydroxides. Accordingly, the release of pollutant s in a
coastal system may not necessarily mean that the sediment
will become polluted. However, in the presence of pollution
sources, confinement and eutrophication may contribute to the
significant increase of pollutants in sediment.
Conclusion
This investigation documents the possible factors that influ-
ence the distribution of toxic metals in the anthropized coastal
Aveiro Lagoon (Portugal). These results indicate that concen-
trations of metals in this lagoon are affected by the anthropo-
genic contributions, the sedimentary dynamics and the bio-
geochemical and related initial diagenetic processes. The
strong tidal influence redistributes sediment-bound metals,
producing a dilution effect in the most hydrodynamical zones.
This is in contrast with an effect of accumulation in areas
affected by low current activity, w here fine-grained sedi-
ment enriched in organic matter is deposited. The rivers
are the main sour ces of metals introduced into Ri a de
Aveiro. Accordingly, the confined areas located in the
vicinity of the river mouths constitute hotspots of contam-
ination. The precipitation of Mn hydroxides and pyrite
formation seem to be important p rocesses i nvolved in
metal retention. This work provides evidence that pollu-
tion in coastal areas is not just related to the supply of
pollutants, as many places in Ria de Aveiro are not pol-
luted, despite their proximity to the sources of pollutants.
Other phen omena, such as hydrodynamical processes
favouring clay minerals and TOC deposition, may con-
tribute to metal increases in surface sediment. The amount
of TOC supplied to the bottom of the lagoon and, in
particular, the intensity of the biogeochemical processes
responsible for the initial diagenetic processes have an
important role in pollution increases, as do the occurrence
of active oxic/anoxic sedimentary boundaries (with pyrite
and/or Mn hydroxide formation and metal retention).
Acknowledgments The authors would like to thank the Editor o f
ESPR, Prof. Céline Guéguen and the reviewer for their collaboration in
the manuscript improvement.
Financial support This work was partially supported by the project
PEst-OE/CTE/UI4035/2014 of the da BFou ndation for Science and
Technology^ (FCT), Portugal, and the project (401803/2010-4) of the
BNational Counsel of Technological and Scientific D evelopment^
(CNPq), Brazil, and the fellowship assigned by PROTEC program, of
BUniversidade do Estado do Rio de J aneiro^ (UERJ , Brazil) and
BUniversidade do Estado do Amazonas^ (UEA; Brazil) to the first author.
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