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Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere
Department of Ecology, Biogeochemistry, and Environmental Protection, University of Wrocaw, ul. Kanonia 6/8, 50-328, Wrocaw, Poland
Department of Chemistry, Norwegian University of Science and Technology, NO-7491, Trondheim, Norway
Independent Chair of Biotechnology and Molecular Biology, Opole University, ul. Kardynaa B. Kominka 6, 45-032, Opole, Poland
h i g h l i g h t s
As, Ba, Fe, Mn, Pb, Ti, U, Zn in mosses reect their level in uranium mine sewages.
Native mosses contained higher metal levels than transplants in more polluted streams.
In less polluted sites reverse situation was observed.
Bioindication in extremely polluted sites may be miscalculated using transplants.
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 31 July 2016
Received in revised form
22 October 2016
Accepted 30 October 2016
Available online xxx
The past uranium/polymetallic mining activities in the Sudety (SW Poland) left abandoned mines, pits,
and dumps of waste rocks with trace elements and radionuclides which may erode or leach out and
create a potential risk for the aquatic ecosystem, among others. In the present work four rivers affected
by efuents from such mines were selected to evaluate the application of aquatic mosses for the bioindication of 56 elements. Naturally growing F. antipyretica and P. riparioides were compared with
transplanted samples of the same species. The results demonstrate serious pollution of the examined
rivers, especially with As, Ba, Fe, Mn, Pb, Ti, U and Zn, reaching extremely high concentrations in native
moss samples. In the most polluted rivers native F. antipyretica and P. riparioides samples showed
signicantly higher concentrations of As, Ba, Cu, Fe, La, Nd, Ni, Pb, U and Zn than corresponding transplanted samples, whereas at less polluted sites a reverse situation was sometimes observed. Transplanted moss moved from clean to extremely polluted rivers probably protects itself against the
accumulation of toxic elements by reducing their uptake. Selection of native or transplanted
F. antipyretica and P. riparioides depended on the pollution load.
2016 Published by Elsevier Ltd.
1. Introduction
The Sudety mountain range (SW Poland) is characterized by its
* Corresponding author.
E-mail addresses: grzegorz.kosior@uwr.edu.pl (G. Kosior), eiliv.steinnes@ntnu.
no (E. Steinnes), aleksandra.samecka-cymerman@uwr.edu.pl (A. Samecka o
czuk-Sr
dka), ziembik@uni.opole.pl
Cymerman), agna@uni.opole.pl (A. Dohan
(Z. Ziembik).
1
Dr. Krzysztof Kolon, our sincere, reliable and irreplaceable friend and coauthor
passed away.
http://dx.doi.org/10.1016/j.chemosphere.2016.10.131
0045-6535/ 2016 Published by Elsevier Ltd.
Please cite this article in press as: Kosior, G., et al., Trace elements in native and transplanted Fontinalis antipyretica and Platyhypnidium
riparioides from rivers polluted by uranium mining, Chemosphere (2016), http://dx.doi.org/10.1016/j.chemosphere.2016.10.131
leaking from the sites, and remains of once mined uranium ores,
such as abandoned pits and dumps of waste rocks, may lead to
erosion and leaching of trace elements and radionuclides and
pollution of aquatic ecosystems (Grabas, 2009; Pala et al., 2013;
Ciszewski et al., 2014). In such environments, mosses are important members of nutrient webs (Rau et al., 2007). These plants have
an ability to accumulate various xenobiotics and thus reect their
level in the geochemical environment (Vincent et al., 2001; Kos
et al., 2010). The pioneering investigations on biogeochemical
prospecting utilizing bryophytes carried on by Whitehead and
Brooks (1969), Brooks (1971), Shacklette and Erdman (1982), and
later Samecka-Cymerman (1994), Samecka-Cymerman and Kempers (1992, 1993, 1994) showed that mosses may dene mineralization more precisely than analyses of water or bottom sediments.
These authors found a relation between the concentration of
metals in aquatic bryophytes and arsenic, barite, uorite, and polymetallic mineralization areas in the Polish and Czech Sudety
mountains. Mosses are widely distributed in the northern hemisphere, stationary, long living, and available all year, with capacity
to trap xenobiotics and relative tolerance to contamination
(Martins et al., 2004; Daz et al., 2013). The aquatic mosses Fontinalis antipyretica Hedw. and Platyhypnidium riparioides (Hedw.)
Dixon selected for the present investigation have these capabilities
and were used as bioindicators in many studies (Carballeira and
pez, 1997; Carballeira et al., 1998; Va
zquez et al., 2000; Cesa
Lo
et al., 2010; Gapeeva et al., 2010; Mechora et al., 2012; Daz et al.,
2013; Kosior et al., 2015). Both species are euryecious with an
ability to characterise the quality of contaminant-affected water
-Alvaro
(Garca
et al., 2000). Thus, the concentration of e.g. metals or
radionuclides in their tissues may indicate the level of environzquez
mental risk caused by pollution (Ceschina et al., 2012; Va
et al., 2013). In environmental control native mosses may be used
as passive biomonitors but also as transplants in cases where native
z and Carballeira, 2000). According to
species are absent (Fern
ande
these authors, plants have the ability to adapt to certain environmental conditions. Therefore, in the present work, native and
transplanted F. antipyretica and P. riparioides were compared as to
their capability to accumulate trace elements from rivers affected
by leakage from uranium mines. The tested hypotheses were: 1)
native aquatic F. antipyretica and P. riparioides exposed to polluted
rivers is able to accumulate smaller amounts of trace elements than
the species transplanted from a site relatively free from pollution;
2) F. antipyretica accumulates greater amounts of trace metals than
P. riparioides when growing in the same river.
2. Materials and methods
2.1. Sampling design
In polymetallic/uranium-rich bedrock sites in the Sudety
mountains (Fig. 1), four rivers were selected in which autochthonous F. antipyretica occurred naturally together with P. riparioides as
tufts totally submerged and immersed throughout the year (Cesa
et al., 2010). Excavations after the extraction of polymetallic deposits, including uranium, penetrate and collect most of the underground inltration water over large areas. A constant outow of
mine water is observed at the outlets of some tunnels. Below such
outlets sampling sites for this investigation were selected. These
were sites in two rivers in the vicinity of Kowary: Jedlica (no. 1e5)
and Jelenia Struga (no. 6e10), in the Klesnica river in the vicinity of
Kletno (no. 11e15) and in the Kamienica river in the vicinity of a
village of Kamienica (no. 16e20). The control site was situated in
zquez et al., 2004), which is
the Kwisa spring area (Fig. 1) (Va
relatively free from pollution. In each river, ve sampling sites
located within 500 m downstream from the source of mine
Please cite this article in press as: Kosior, G., et al., Trace elements in native and transplanted Fontinalis antipyretica and Platyhypnidium
riparioides from rivers polluted by uranium mining, Chemosphere (2016), http://dx.doi.org/10.1016/j.chemosphere.2016.10.131
Fig. 1. Location of the investigated area. Symbols: full squares sampling sites in polluted Jedlica (1e5), Jelenia Struga (6e10), Klesnica (11e15) and Kamienica (16e20) rivers; open
square control sites in the source area of Kwisa.
Please cite this article in press as: Kosior, G., et al., Trace elements in native and transplanted Fontinalis antipyretica and Platyhypnidium
riparioides from rivers polluted by uranium mining, Chemosphere (2016), http://dx.doi.org/10.1016/j.chemosphere.2016.10.131
0.21, Zr 0.48.
The differences between concentrations of trace elements in
mosses from different sites were evaluated by ANOVA (Zar, 1999).
The signicance of differences in trace element concentrations
between control and native or transplanted F. antipyretica and
P. riparioides were compared with the t-test.
A post-hoc LSD test was used to compare metal concentrations
in mosses between four different rivers.
Pearson correlations between concentrations of trace elements
in native and transplanted F. antipyretica and P. riparioides were
calculated.
All calculations were carried out using Statistica 12 software
(StatSoft Inc, 2014).
3. Results and discussion
The descriptive statistics of trace element ranges in
F. antipyretica and P. riparioides from four rivers and the control are
listed in Electronic Supplementary Material (ESM) 1e5. The mean
concentrations of these elements in mosses from different sites
differed signicantly (ANOVA, P < 0.05) between the rivers.
Trace element concentrations in the native and transplanted
F. antipyretica and P. riparioides were higher in comparison to the
control samples (t-test, P < 0.05). The upper values also exceeded
the concentrations (mg g1) of Al (2666), Ba (81), Be (0.7), Ce (11), Co
(3.6), Cr (4.1), Cu (10), Fe (3757), Hg (0.06), Mn (849), Mo (0.7), Ni
(8.8), Pb (7.4), Rb (11), Sr (23), Ti (114), Tl (0.07), V (6.6), and Zn (130)
zquez et al. (2000) as typical for F. antipyretica from
presented by Va
_
unpolluted spring parts of the Nysa uzycka
river (SW Poland). In
addition, As concentrations were much higher than 1.1 mg g1 given
by Culioli et al. (2009) for F. antipyretica from clean sites. Favas et al.
(2014) considered 3.8 mg g1 as a background water moss concentration of U and observed up to 4979 mg g1 of this element in
F. antipyretica from uranium mineralized areas in Portugal. Native
F. antipyretica and P. riparioides from the most polluted Jedlica river
(sites 1e10) contained much higher concentrations up to (mg g1)
577 and 409 of uranium, respectively (ESM 1). These results point
to the serious pollution of the examined river especially with As, Ba,
Fe, Mn, Pb, Ti, U and Zn reaching extremely high concentrations in
native F. antipyretica and P. riparioides (ESM 1e2).
The T-test (P < 0.05) revealed that control F. antipyretica contained signicantly higher concentrations of Be, Cu, Er, Ge, Hg, Ho,
La, Mn, Mo, Nd, Ni, Pb, Pr, Sb, Sm, Sr, Ta, Tl, U, V, W, Yb, Zn and Zr and
signicantly lower concentrations of Cs, Fe, Hf, Nb, Si, Th and Ti
than P. riparioides from the same sites. Native mosses did not differ
in the concentration of these elements except for Th, which was
also higher in native P. riparioides. For transplants of both species,
the same relations as in the control river were observed for Er, Ge,
Mo, Sb, Sr Ta, Tl Yb and Zn. According to Siebert et al. (1996) and
Wehr and Whitton (1983), P. riparioides is more sensitive to changes
in the concentration of metals in water and can accumulate Cd, Cu,
Fe, Pb and Zn at higher levels than F. antipyretica. In the present
investigation, P. riparioides accumulated more Fe than F. antipyretica
according to the aforementioned report but less Cu, Pb, and Zn than
F. antipyretica. This discrepancy may be caused by the fact that the
above authors measured metals in 2 cm tips of mosses. Wehr and
Whitton (1983) state that the best control of differences in metalbinding properties of both species might be obtained in populations collected (as in this investigation) from the same river.
Similar accumulation patterns of some trace elements in
F. antipyretica, being higher than in P. riparioides both in the control
river as well as in the same mosses transplanted to the polluted
rivers, may probably be explained by some memory effect (Mouvet
et al., 1993; Ogle et al., 2015). However, further investigation is
necessary to probe into this problem.
Please cite this article in press as: Kosior, G., et al., Trace elements in native and transplanted Fontinalis antipyretica and Platyhypnidium
riparioides from rivers polluted by uranium mining, Chemosphere (2016), http://dx.doi.org/10.1016/j.chemosphere.2016.10.131
Please cite this article in press as: Kosior, G., et al., Trace elements in native and transplanted Fontinalis antipyretica and Platyhypnidium
riparioides from rivers polluted by uranium mining, Chemosphere (2016), http://dx.doi.org/10.1016/j.chemosphere.2016.10.131
Press, Cambridge.
Grabas, K., 2009. Environmental hazard in the area of the former uranium ore mine
rze in Kowary. Environ. Prot. Eng. 35, 127e137.
Podgo
Harmens, H., Foan, L., Simon, V., Mills, G., 2013. Terrestrial mosses as biomonitors of
atmospheric POPs pollution: a review. Environ. Pollut. 173, 245e254.
Kaszubkiewicz, J., Kawako, D., 2009. Total content of heavy metals in soils and
ra district. Ochr. Srodowiska
w Nat. 40,
plants at the area of Jelenia Go
Zasobo
177e189.
Kos, A., Rajfur, M., Wacawek, M., Wnschmann, W., Wnschmann, S., Markert, B.,
2010. Quantitative relations between different concentrations of micro- and
macroelements in mosses and lichens: the region of Opole (Poland) as an
environmental interface in between Eastern and Western Europe. Int. J. Environ. Health 4, 98e119.
Koleva, D., Stefanova, M., Ganeva, Ts, 2014. Ultrastructural responses of the leaves of
Fontinatis antipyretica Hedw. to copper and cadmium. Oxid. Commun. 37,
392e399.
ska-Kosior, A., Bena, W.,
Kosior, G., Samecka-Cymerman, A., Kolon, K., Brudzin
Kempers, A.J., 2015. Trace elements in the Fontinalis antipyretica from rivers
receiving sewage of lignite and glass sands mining industry. Environ. Sci. Pollut.
Res. 22, 9829e9838.
Kosior, G., Samecka-Cymerman, A., Kolon, K., Kempers, A.J., 2010. Bioindication
capacity of metal pollution of native and transplanted Pleurozium schreberi
under various levels of pollution. Chemosphere 81, 321e326.
Kryza, R., Pin, Ch, 2010. The Central-Sudetic ophiolites (SW Poland): petrogenetic
issues, geochronology and palaeotectonic implications. Gondwana Res. 17,
292e305.
Lodenius, M., Tulisalo, E., Soltanpour-Gargari, A., 2003. Exchange of mercury between atmosphere and vegetation under contaminated conditions. Sci. Total
Environ. 304, 169e174.
Marszaek, H., Wa sik, M., 2000. Inuence of arsenic-bearing gold deposits on water
quality in Zloty Stok mining area (SW Poland). Environ. Geol. 39, 888e892.
Martins, R.J., Pardo, R., Boaventura, R.A., 2004. Cadmium(II) and zinc(II) adsorption
by the aquatic moss Fontinalis antipyretica: effect of temperature, pH and water
hardness. Water Res. 38, 693e699.
Germ, M., Stibilj, V., 2012. Selenium and its species in the aquatic moss
Mechora, S.,
Fontinalis antipyretica. Sci. Total Environ. 438, 122e126.
Mochnacka, K., Banas, M., 2000. Occurrence and genetic relationship of uranium
and thorium mineralization in the Karkonosze-Izera Block (the Sudety Mts.,
SWPoland). Ann. Soc. Geol. Pol. 70, 137e150.
Mochnacka, K., Oberc-Dziedzic, T., Mayer, W., Pieczka, A., 2015. Ore mineralization
related to geological evolution of the KarkonoszeeIzera Massif (the Sudetes,
Poland) d towards a model. Ore Geol. Rev. 64, 215e238.
Mouvet, C., 1984. Accumulation of chromium and copper by the aquatic moss
Fontinalis antipyretica L. ex Hedw. transplanted in a metal-contaminated river.
Envir. Technol. Lett. 5, 541e548.
Mouvet, C., Morhain, E., Sutter, C., Couturieux, N., 1993. Aquatic mosses for the
detection and follow-up of accidental discharges in surface waters. Water Air
Soil Pollut. 66, 333e348.
Ogle, K., Barber, J.J., Barron-Gafford, F.A., Bentley, L.P., Young, J.M., Huxman, T.E.,
Loik, M.E., Tissue, D.T., 2015. Quantifying ecological memory in plant and
ecosystem processes. Ecol. Lett. 18, 221e235.
ska, J., 2013. Content analysis of
Pala, A., Widziewicz, K., Nowak, J., Loska, K., Biegan
heavy metals/metalloids and mineral composition of waste generated during
uranium concentrate processing. Gospod. Surowcami Min. 29, 89e102.
Rao, D.N., 1982. Responses of Bryophytes to air pollution. In: Smith, A.J.E. (Ed.),
Bryophyte Ecology. Chapman and Hall, London, pp. 445e471.
Rau, S., Miersch, J., Neumann, D., Weber, E., Krauss, G.J., 2007. Biochemical responses
of the aquatic moss Fontinalis antipyretica to Cd, Cu,Pb and Zn determined by
Please cite this article in press as: Kosior, G., et al., Trace elements in native and transplanted Fontinalis antipyretica and Platyhypnidium
riparioides from rivers polluted by uranium mining, Chemosphere (2016), http://dx.doi.org/10.1016/j.chemosphere.2016.10.131