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Effects of activated carbon on PCB bioaccumulation and biological responses of Chironomus riparius in full life cycle test Inna Nybom, Sebastian Abel, Greta Catherine Waissi, Kristiina Väänänen, Kimmo Mäenpää, Matti T. Leppanen, Jussi V.K. Kukkonen, and Jarkko Akkanen Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b00991 • Publication Date (Web): 21 Apr 2016 Downloaded from http://pubs.acs.org on April 24, 2016
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Environmental Science & Technology
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Effects of activated carbon on PCB bioaccumulation and biological responses of Chironomus
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riparius in full life cycle test
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Inna Nybom*1, Sebastian Abel1, Greta Waissi1, Kristiina Väänänen1, Kimmo Mäenpää1, Matti T.
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Leppänen2, Jussi V.K. Kukkonen3, Jarkko Akkanen1
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Box 111, FI-80101 Joensuu, Finland
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FI-40014 University of Jyväskylä, Finland.
Department of Environmental and Biological Sciences, University of Eastern Finland (UEF), P.O.
Finnish Environment Institute (SYKE), Ecotoxicology and risk assessment group, P.O. Box 35,
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40014 University of Jyväskylä, Finland.
University of Jyväskylä, Department of Biological and Environmental Science, P.O. Box 35, FI-
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[email protected] 14 15
ABSTRACT
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The nonbiting midge Chironomus riparius was used to study the remediation potential and
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secondary effects of activated carbon (AC, ø 63–200 µm) in PCB contaminated sediments. AC
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amendments efficiently reduced PCB bioavailability determined by C. riparius bioaccumulation
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tests and passive samplers. PCBs were shown to transfer from larvae to adults. Lower PCB
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concentrations were observed in adult midges emerging from AC amended compared to unamended
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sediments. Increased reproduction, survival, larval growth and gut wall microvilli length were
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observed with low AC dose (0.5% sediment dw) compared to unamended sediment, indicating an
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improved success of larvae in the sediment with low organic carbon content. On the other hand,
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higher AC doses (2.5% sediment dw) caused adverse effects on emergence and larval development.
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In addition, morphological changes in the gut wall microvilli layer were observed. This study
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showed that the secondary effects of AC amendments are dependent on the dose and the sediment
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characteristics. Metamorphic species, such as C. riparius, may act as a vector for organic pollutants
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from aquatic to terrestrial ecosystems and according to this study the AC amendments may reduce
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this transport.
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INTRODUCTION
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Several studies have shown that activated carbon (AC) efficiently reduces aqueous and
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bioaccumulated concentrations of hydrophobic organic compounds (HOCs), e.g. polychlorinated
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biphenyls
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dichlorodiphenyltrichloroethanes (DDTs),8-10 dioxins11,
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(TBT).13
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Along with the remedial effects, secondary effects, e.g. reduced weight or inhibited growth
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and decreased lipid content,16, 19, 20 has been reported for several benthic invertebrates. Sediment-
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dwelling organisms such as Lumbriculus variegatus have been shown to be especially sensitive to
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AC amendments,16, 18, 19, 21 and adverse effects, including morphological changes to the gut wall
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microvilli layer,18 have been reported at doses lower than generally recommended for remedial
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purposes (1–5%).22 The results relating to secondary effects are contradictory, and some studies
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have shown no effects on biological endpoints such as growth,12, 14, 15, 17, 20 lipid content5, 12, 14, 17, 20
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or avoidance behavior.15,
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experiments due to reduced sediment toxicity.15 The biological responses have been recently
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reviewed by Janssen and Beckingham (2013),23 and Kupryianchyk et al. (2015).24
(PCBs),1-5
polycyclic
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aromatic
hydrocarbons 12
(PAHs),1,
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and organotins, such as tributyltin
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Some positive effects on survival have been reported in short-term
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Within this study, the effects of AC amendments on PCB bioaccumulation and
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secondary responses were studied with Chironomus riparius, a nonbiting midge with a four-stage
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lifecycle: egg, larva, pupa and adult midge. Chironomids spend 90% of their lifespan under aquatic
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conditions (egg, larvae and pupa), of which the sediment-dwelling larvae phase is the longest (70–
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80% of the lifespan).25 Larvae are deposit feeders26 and hence readily exposed to contaminants in
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sediments. Additionally, organisms undergoing metamorphosis may act as a link between aquatic
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and terrestrial ecosystems.27 Organochlorines (e.g. PCBs) have been shown to be retained within the
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insect body during metamorphosis, which leads to increased concentrations in adults, which have
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smaller mass than the larvae.28-30 Benthic organisms exposing directly to sediment associated
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particles, have been shown to be sensitive to AC amendments.16 Therefore C. riparius is relevant
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tests species to study the secondary effects of AC, and the effects seen in larvae may accumulate to
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the following developmental stages. Changes at the bottom of the food webs may alter the food web
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structure and also the food chain transfer of HOCs.31
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The present study investigated the effects of AC amendment on the bioavailability of
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PCBs in two field-collected sediments. Bioavailability was evaluated using C. riparius larvae, adult
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midges, and passive samplers. The secondary effects of AC amendments were studied in a 10-day
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larvae growth test and in a full lifecycle test over two generations. The studied endpoints were
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growth and developmental stage of the larvae, emergence time, developmental rate, sex ratio and
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egg production in the full lifecycle test. Additionally, transmission electron microscopic (TEM)
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samples were prepared from the larvae exposed for 10 days in order to study morphological
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changes in gut wall microvilli layer.
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MATERIALS AND METHODS
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Organisms
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C. riparius were cultured at the University of Eastern Finland in the Department of Biology. The
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rearing method has been described earlier by Waissi-Leinonen et al. (2012).32 Midges were
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collected from the culture for mating five to seven days prior to the experiments. The midges laid
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several egg ropes, and hatched first instar larvae (≤ 3 d post-hatch) were used in the experiments.
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Sediments
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Two natural sediments collected from PCB-contaminated areas were used in the experiments:
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River Tervajoki (N 60° 82' 34'' E 24° 63' 52'', TJ) and Lake Kernaalanjärvi (N 60° 85' 44'' E 24° 64'
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21'', KJ), both locating in the same water body. The PCB contamination relates to discharges of
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PCB oils from a paper mill from 1956 to 1984.31 The sediments were sieved to a particle size of
