Exposure to sediments from polluted rivers has limited phenotypic effects on larvae and adults of Chironomus riparius
Introduction
Rivers contaminated by metals and organic substances have often been reported to be associated with an increased incidence of phenotypic defects, such as phenodeviation and fluctuating asymmetry (FA), particularly in invertebrates (Al-Shami et al., 2011; Bonada and Williams, 2002, Groenendijk et al., 1998). A phenodeviation is an abnormal and rare expression of a trait (Lerner, 1954, Rasmuson, 1960) while fluctuating asymmetry refers to random and subtle departure from a perfect bilateral symmetry (van Valen, 1962). These morphological defects occur when developmental homeostasis is insufficient to compensate environmental stress (Graham et al., 1993, Palmer and Strobeck, 1992) and have thus been proposed as relevant indicators of such environmental stress (Leary and Allendorf, 1989, Vermeulen, 1995). Particularly, phenodeviations have been widely reported in chironomid larvae (Diptera) collected in rivers contaminated by metals (Janssens de Bisthoven et al., 1998a, Martinez et al., 2002) or organic compounds (Janssens de Bisthoven et al., 1996, Servia et al., 1998). Among the chironomid larvae, the genus Chironomus (Al-Shami et al., 2011, Bird, 1994, Di Veroli et al., 2012, Janssens de Bisthoven et al., 1998a, Lenat, 1993), particularly the species Chironomus riparius (Servia et al., 1998), has been shown to be prone to such pollution-induced phenotypes.
To identify the substances involved in phenotypic defects and the concentrations necessary to induce them, numerous bioassays have been performed in C. riparius larvae under controlled conditions in the laboratory (Bleeker et al., 1999, Di Veroli et al., 2012, Meregalli et al., 2001, Park et al., 2009). This species has been widely used for sediment bioassay for several reasons. First, the larvae spend the majority of their life in sediment making them particularly relevant for sediment bioassay. Second, the abundance of this species in both preserved and disturbed rivers facilitates the sampling of numerous individuals. Third, C. riparius can be easily cultured in the laboratory (short life cycle, resistance to manipulation), allowing to perform bioassay in controlled conditions. Fourth, as C. riparius is one of the most commonly used species (Groenendijk et al., 1998, Watts et al., 2003, Park et al., 2009, Servia et al., 2004 Vogt et al., 2013), a good comparative framework is available. Despite this common use in ecotoxicological studies, the phenotypic responses of Chironomus larvae to pollution are heterogeneous across studies: while some studies have reported increased frequency of deformities and FA following an exposure to mineral (Martinez et al., 2003) or organic compounds (Meregalli et al., 2001, Park et al., 2009), others failed to detect such effects (Arambourou et al., 2012, Bird et al., 1995).
Several hypotheses have been proposed to explain the weak link observed between stress and phenotypic defects in laboratory studies, as discussed in Arambourou et al. (2012). First, developmental stability in aquatic invertebrates could be mainly affected by a combination – rather than a single – of stressful environmental conditions (Campero et al., 2008, Langer-Jaesrich et al., 2010). Indeed, the use of a single pollutant – as it is often the case in the laboratory – could be inefficient in inducing strong phenotypic effects. Second, to explain the weak responses measured in the larval life stage of a damselfly, Campero et al. (2008) proposed that, as metamorphosis is energetically costly and thus comparable to a stressful event, FA could be higher in adults than in larval life stages, suggesting that adults should be preferentially used to detect developmental instability. Third, morphological abnormalities could appear after several generations of exposure. Indeed, it is well known now that some toxics, such as endocrine disruptors, can contribute to trans-generational developmental effects in aquatic organisms, such as in the fish Oryzias latipes (Gray et al., 1999, Zhang et al., 2008), leading to an increase of morphological abnormalities in the offspring derived from the exposed parents. In the present study, we test these three hypotheses in C. riparius exposed to sediments collected in multi-contaminated rivers.
Section snippets
Experimental design
The experiment consisted of exposing laboratory C. riparius larvae during their entire larval life cycle to two sediments sampled in disturbed rivers (Fig. 1). First, to test whether a multiple toxic exposure would have severe phenotypic effects, we exposed larvae to sediments collected in disturbed rivers and those containing a mixture of mineral and organic compounds. In the larvae, after 20 days of exposure, we measured three types of mentum phenotypic variations: the frequency of
Characterization of the three sediments studied
By comparison with both the control and the LOW sediment (Supplementary material 1, Table A), the HIGH sediment showed high levels of organic matter, organic carbon, organic nitrogen and total phosphorus. The ratio between organic carbon and organic nitrogen is between 8 and 14 in LOW and HIGH sediments. This result suggested that unlike the control sediment, a part of the organic matter is available for the feeding of the chironomid larvae (Péry et al., 2003) in the field-collected sediments.
Polluted sediments can impact body dry weight and induce growth retardation
We detected high heavy metal concentrations in the body of the larvae from the HIGH sediment (similar concentrations were reported in the literature; Di Veroli et al., 2012, Krantzberg and Stockes, 1989, Roulier et al., 2008). These high concentrations were accompanied by a reduced larval dry weight and a delayed development (longer time to emergence). Similar results have been obtained in Chironomus larvae exposed to organic (Watts et al., 2003) or mineral (Pascoe et al., 1989, Postma et al.,
Conclusions
In conclusion, as observed in a previous study (Arambourou et al., 2012), we detected only limited phenotypic effects in C. riparius exposed to contaminated sediments. To explain the weak phenotypic response observed in the present study, four hypotheses could be proposed. First, FA and deformities might not be the relevant indicators of toxic exposure that they are often claimed. This idea has been already proposed to explain the contradictory results observed in the literature (e.g. Leung et
Acknowledgment
This investigation was supported by the French Ministry of Ecology, Sustainable Development and Energy and by the French Institute of Science and Technology for Transport, Development and Networks.
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