Elsevier

Science of The Total Environment

Volume 484, 15 June 2014, Pages 92-101
Science of The Total Environment

Exposure to sediments from polluted rivers has limited phenotypic effects on larvae and adults of Chironomus riparius

https://doi.org/10.1016/j.scitotenv.2014.03.010Get rights and content

Abstract

Laboratory studies have sometimes failed to detect a relationship between toxic stress and morphological defects in invertebrates. Several hypotheses have been proposed to account for this lack of effect. (1) It was suggested that only a combination of stressful conditions – rather than a single one – would affect the phenotype. (2) Phenotypic defects should be detected on adult individuals, rather than on juveniles. (3) Phenotypic abnormalities might mostly affect the progeny of the exposed individuals, some contaminants exhibiting trans-generational effects. In the present study, we test those three hypotheses. We first examined the effects of a multiple exposure by using laboratory Chironomus riparius larvae cultured on two sediments sampled in contaminated rivers and those containing a mixture of mineral and organic compounds. On the larvae, we investigated mentum phenotypes: the frequency of phenodeviants, the shape fluctuating asymmetry and the mean shape. To test whether adult's morphology was more sensitive than the larval's, we also measured asymmetry and mean shape of the adult wings. Finally, to test for a trans-generational phenotypic effect, we measured mentum shape variations in the offspring derived from the measured adults. Overall, our results point out a very limited phenotypic response to contaminated sediments, suggesting that a multiple exposure is not necessarily sufficient to generate phenotypic defects. Adult traits were no more affected than larval traits, discarding the hypothesis that adult phenotypes would be more sensitive biomarkers. Finally, no effect was detected on the offspring generation, suggesting that no trans-generational effect occurs. This general lack of effect suggests that the use of phenotypic defects in C. riparius as an indicator of sediment contamination should be considered cautiously.

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.

References (67)

  • J.L. Roulier et al.

    Measurement of dynamic mobilization of trace metals in sediments using DGT and comparison with bioaccumulation in Chironomus riparius: first results of an experimental study

    Chemosphere

    (2008)
  • M.M. Watts et al.

    Exposure to 17α-ethinylestradiol and bisphenol-A — effects on larval moulting and mouthpart structure of Chironomus riparius

    Ecotoxicol Environ Saf

    (2003)
  • P. Alibert et al.

    Genomic coadaptation, outbreeding depression, and developmental instability

  • S.A. Al-Shami et al.

    Fluctuating asymmetry of Chironomus spp. (Diptera: Chironomidae) larvae in association with water quality and metal pollution in Permatang Rawa river in the Juru River Basin, Penang, Malaysia

    Water Air Soil Pollut

    (2011)
  • H. Arambourou et al.

    Patterns of fluctuating asymmetry and shape variation in Chironomus riparius (Diptera, Chironomidae) exposed to nonylphenol or lead

    PLoS One

    (2012)
  • H. Arambourou et al.

    Biochemical and morphological responses in Chironomus riparius (Diptera, Chironomidae) larvae exposed to lead spiked sediment

    Environ Toxicol Chem

    (2013)
  • G.A. Bird

    Use of chironomid deformities to assess environmental degradation in the Yamaska River, Quebec

    Environ Monit Assess

    (1994)
  • G.A. Bird

    Deformities in cultured Chironomus tentans larvae and the influence of substrate on growth, survival and mentum wear

    Environ Monit Assess

    (1997)
  • G.A. Bird et al.

    The effect of 210Pb and stable lead on the induction of menta deformities in Chironomus tentans larvae and on their growth and survival

    Environ Toxicol Chem

    (1995)
  • E.A.J. Bleeker et al.

    Effect of exposure to azaarenes on emergence and mouthpart development in the midge Chironomus riparius (Diptera: Chironomidae)

    Environ Toxicol Chem

    (1999)
  • N. Bonada et al.

    Exploration of the utility of fluctuating asymmetry as an indicator of river pollution using larvae of the caddisfly Hydropsyche morosa (Trichoptera: Hydropsychidae)

    Hydrobiologia

    (2002)
  • F.L. Bookstein

    Morphometric tools for landmark data: geometry and biology

    (1991)
  • M. Campero et al.

    Metamorphosis offsets the link between larval stress, adult asymmetry and individual quality

    Funct Ecol

    (2008)
  • G.M. Clarke

    The genetic basis of developmental stability. Individual and population asymmetry parameters

    Heredity

    (1998)
  • V. Debat et al.

    Independence between developmental stability and canalization in the skull of the house mouse

    Proc R Soc

    (2000)
  • J.H. Epler

    Identification manual for the larval Chironomidae (Diptera) of North and South Carolina

    (2001)
  • N. Friberg et al.

    Stream macroinvertebrate occurrence along gradients in organic pollution and eutrophication

    Freshw Biol

    (2010)
  • A.M. Gower et al.

    Water quality and the occurrence of Chironomus riparius Meigen (Diptera: Chironomidae) in a stream receiving sewage effluent

    Freshw Biol

    (1978)
  • J.H. Graham et al.

    Developmental stability and its application in ecotoxicology

    Ecotoxicology

    (1993)
  • M.A. Gray et al.

    Reproductive success and behaviour of Japanese medaka, Oryzias latipes exposed to 4-tert-octylphenol

    Environ Toxicol Chem

    (1999)
  • D. Groenendijk et al.

    Fluctuating asymmetry and mentum gaps in populations of midge Chironomus riparius (Diptera: Chironomidae) from a metal contaminated river

    Environ Toxicol Chem

    (1998)
  • A.A. Hoffmann et al.

    Wing shape versus asymmetry as an indicator of changing environmental conditions in insect

    Aust J Entomol

    (2005)
  • L. Janssens de Bisthoven et al.

    Field and experimental morphological response of Chironomus larvae (Diptera: Nematocera) to xylene and toluene

    Neth J Zool

    (1996)
  • Cited by (27)

    • Accumulation of As, Cd, Pb, and Zn in sediment, chironomids and fish from a high-mountain lake: First insights from the Carnic Alps

      2020, Science of the Total Environment
      Citation Excerpt :

      This reflects the concentration levels recorded in Diptera Chironomidae, since it is an important taxon of sediment-bound contaminants (Hudson and Ciborowski, 1996). Chironomidae larvae spend most of their life in close contact with the sediment, making this taxon particularly relevant for biomonitoring studies (Arambourou et al., 2014). Arslan et al. (2010) also found that chironomids accumulate metals several times over their surrounding environment (e.g., sediment), which explains the higher concentration we recorded.

    • Is developmental instability in chironomids a sensitive endpoint for testing uranium mine-affected sediments?

      2020, Science of the Total Environment
      Citation Excerpt :

      We recommend that time to emergence should be used as an indicator of developmental effects in further studies with Chironomus. The usefulness of this endpoint is supported by the findings of other studies (Arambourou et al., 2014, 2019). The approach used in this study (controlled laboratory experiments with sediments from a contaminated site) avoids confounding due to uncontrolled environmental variables and adaptation to long-term contamination, which may mask effects on natural populations.

    • Exposure to heavy metal-contaminated sediments disrupts gene expression, lipid profile, and life history traits in the midge Chironomus riparius

      2020, Water Research
      Citation Excerpt :

      After emergence, adults were collected and sexed, their wings removed and placed on microscope slides in Eukitt® medium and then scanned using a Plustek OpticFilm 7400 scanner. Wing shape variations were measured by geometric morphometrics after digitizing 8 “type 1” landmarks, according to Arambourou et al. (2014). Wing area was calculated as the polygon delimited by the landmarks 1, 2, 3, 4, 5 and 8.

    View all citing articles on Scopus
    View full text