Aquatic Toxicology 154 (2014) 1–11
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Aquatic Toxicology
j ourna l ho me pa ge: www.elsevier.com/locate/aquatox
Effects of depleted uranium on the reproductive success and F1
generation survival of zebrafish (Danio rerio)
Stéphanie Bourrachot
a
, Franc ¸ ois Brion
b
, Sandrine Pereira
a
, Magali Floriani
a
,
Virginie Camilleri
a
, Isabelle Cavalié
a
, Olivier Palluel
b
, Christelle Adam-Guillermin
a,∗
a
Institut de Radioprotection et de Sûreté Nucléaire (IRSN), PRP-ENV/SERIS/LECO, Cadarache, Saint-Paul-lez-Durance 13115, France
b
Institut National de l’Environnement Industriel et des Risques (INERIS), Unité d’évaluation des risques écotoxicologiques, BP2,
60550 Verneuil-en-Halatte, France
a r t i c l e i n f o
Article history:
Received 15 January 2014
Received in revised form 1 April 2014
Accepted 12 April 2014
Available online 21 April 2014
Keywords:
Uranium
Zebrafish (Danio rerio)
Reproduction
Genotoxicity
Parental exposure
a b s t r a c t
Despite the well-characterized occurrence of uranium (U) in the aquatic environment, very little is known
about the chronic exposure of fish to low levels of U and its potential effect on reproduction. Therefore,
this study was undertaken to investigate the effects of environmental concentrations of depleted U on
the reproductive output of zebrafish (Danio rerio) and on survival and development of the F1 embryo-
larvae following parental exposure to U. For that purpose, sexually mature male and female zebrafish
were exposed to 20 and 250 g/L of U for 14 days and allowed to reproduce in clean water during a
further 14-day period. At all sampling times, whole-body vitellogenin concentrations and gonad histol-
ogy were analyzed to investigate the effects of U exposure on these reproductive endpoints. In addition,
accumulation of U in the gonads and its genotoxic effect on male and female gonad cells were quantified.
The results showed that U strongly affected the capability of fish to reproduce and to generate viable
individuals as evidenced by the inhibition of egg production and the increased rate of mortality of the
F1 embryos. Interestingly, U exposure resulted in decreased circulating concentrations of vitellogenin in
females. Increased concentrations of U were observed in gonads and eggs, which were most likely respon-
sible for the genotoxic effects seen in fish gonads and in embryos exposed maternally to U. Altogether,
these findings highlight the negative effect of environmentally relevant concentrations of U which alter
the reproductive capability of fish and impair the genetic integrity of F1 embryos raising further concern
regarding its effect at the population level.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Uranium (U) is naturally found as a mixture of three isotopes:
234
U,
235
U, and
238
U. These isotopes are all alpha emitters and con-
tribute to 0.005%, 0.720% and 99.274% of natural uranium (NU) mass
composition, respectively (Madic and Genet, 2001). U is naturally
present in the earth’s crust at concentrations of 2–4 g t
-1
, and is
dispersed throughout the biosphere in soil, water, air, plants, and
animals through natural biogeochemical processes (Ribera et al.,
1996; Bleise et al., 2003). Natural concentrations of U in water
vary from a few ng L
-1
to more than 12 mg L
-1
(World Health
Organization, 2001; Salonen, 1994). However, U concentrations can
increase due to various anthropogenic contributions, such as indus-
trial activities linked to nuclear fuel production, numerous military
applications (Miller and McClain, 2007), or accidental discharge
∗
Corresponding author. Tel.: +33 4 42 19 94 01; fax: +33 4 42 19 91 51.
E-mail address: christelle.adam-guillermin@irsn.fr (C. Adam-Guillermin).
(Gagnaire et al., 2011). For example, high concentrations of U from
10 to 20 mg L
-1
have been measured in water close to mining sites
in the United States (Ragnarsdottir and Charlet, 2000).
Depleted uranium (DU) is a byproduct of NU enrichment. Its
widespread use in armor-penetrating weapons has raised environ-
mental and human health concerns (World Health Organization,
2001). The (eco)toxicological risks associated with U potentially
originate from both its chemical and radiological properties,
depending on the specific activity of the different isotopes. How-
ever, for DU and NU, the risks are greater due to chemical rather
than radiological toxicity (Mathews et al., 2009).
The ecotoxicological effects of U are not fully known. Studies
describing the effects of U in fish have primarily focused on bioac-
cumulation and acute toxicity induced by waterborne exposure to
U. For instance, lethal concentrations at 50% (LC
50s
) (96 h) ranging
from 0.7 to 135 mg L
-1
have been reported depending on biotic
(species, life stage) and abiotic factors (temperature, water hard-
ness, pH) (Poston, 1982; Bywater et al., 1991; Labrot et al., 1999;
Roex et al., 2002). More recently, it was shown that exposure of
http://dx.doi.org/10.1016/j.aquatox.2014.04.018
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