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Bioconcentration of Organic Contaminants in Daphnia Resting Eggs Aurea C Chiaia-Hernandez, Roman Ashauer, Markus Moest, Tobias Hollingshaus, Junho Jeon, Piet Spaak, and Juliane Hollender Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es401763d • Publication Date (Web): 07 Aug 2013 Downloaded from http://pubs.acs.org on August 13, 2013
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Bioconcentration of Organic Contaminants in Daphnia Resting Eggs
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Aurea C Chiaia-Hernandez1,2, Roman Ashauer1,3, Markus Moest1,4, Tobias Hollingshaus1,
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Junho Jeon1, Piet Spaak1,4 and Juliane Hollender1,2*
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Switzerland
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Institute of Biogeochemistry and Pollutant Dynamics, ETH Zurich, Switzerland
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Environment Department, University of York, Heslington, York, United Kingdom
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Institute of Integrative Biology, ETH Zurich, Switzerland
Eawag, Swiss Federal Institute of Aquatic Science and Technology (Eawag)
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*Corresponding author
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Überlandstrasse 133, PO BOX 611. 8600 Dübendorf, Switzerland; phone: +41 58 765
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5493; fax: +41 58 765 5893; email:
[email protected] 14 15
Abstract
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Organic contaminants detected in sediments from Lake Greifensee and other compounds
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falling in the log Dow range from 1 to 7 were selected to study the bioconcentration of
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organic contaminants in sediments in Daphnia resting eggs (ephippia). Our results show
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that octocrylene, tonalide, triclocarban, and other personal care products, pesticides and
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biocides can accumulate in ephippia with log BCF values up to 3. Data on the uptake and
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depuration kinetics show a better fit towards a two compartment organism model over a
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single compartment model due to the differences in ephippial egg content in the
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environment. The obtained BCFs correlate with hydrophobicity for neutral compounds.
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Independence between BCF and hydrophobicity was observed for partially ionized
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compounds with log Dow values around 1. Internal concentrations in ephippia in the
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environment were predicted based on sediment concentrations using the equilibrium
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partitioning model and calculated BCFs. Estimated internal concentration values ranged
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between 68,000 µg/kglip to 1 µg/kglip with triclocarban having the highest internal
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concentrations followed by tonalide and triclosan. The outcomes indicate that
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contaminants can be taken up by ephippia from the water column or the pore water in the
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sediment and might influence fitness and sexual reproduction in the aquatic key species
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of the genus Daphnia.
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Introduction
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During the last century, most European lakes with anthropogenic point sources went
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through a phase of eutrophication which was accompanied by a shift in species
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composition and diversity of both pelagic and littoral communities, reduction of water
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quality, and even occasional fish kills.1 The installation of sewage treatment plants in the
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1980s2 and their continuous upgrade enabled the recovery of many lakes to their original
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trophic state. Simultaneous to eutrophication, numerous new chemicals have been
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produced for use in households, agriculture, and industry.3 Studies have revealed that
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chemical pollutants influence the aquatic food web,
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which time-scales chemical pollutants are influencing the aquatic food web, as well as the
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extent of the impact is not well known. Measurements of emerging contaminants such as
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pharmaceutical and personal care products (PPCPs) started in the 1990s, thus the
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exposure before is not well studied.
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In our previous work, we showed that sediments can be integrators in time of polar and
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medium polar organic compounds providing historical patterns of chemical deposition.6
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The ability of organic contaminants to sorb to sediments constitutes a primary source of
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exposure for benthic organisms. Benthic organisms can accumulate organic contaminants
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from the particulate and interstitial components of sediments as well as from the water
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column.7,
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mechanisms and bioavailability, given that it is captured during the sedimentation process
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and is essentially isolated from the water column.7, 9
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One of the most important planktonic grazers in pelagic food webs are species of the
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genus Daphnia (Crustacea, Anomopoda; water fleas). Daphnia species serve as food for
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fish and invertebrates, and they feed on algae and bacteria.10 Daphnia normally reproduce
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clonally (parthenogenetic cycle) but they switch to sexual reproduction (sexual cycle)
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when environmental conditions are not ideal and the production of males and sexual eggs
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is then triggered by changes in food level, crowding, and photoperiod.10, 11 Sexual eggs
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are diapause stages, enclosed in a structure called ephippium that can sink to the bottom
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4, 5
but how this is happening and at
Sediment pore water plays an important role in sediment-water sorption
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of the lake and remain there until conditions become more favorable. Ephippia can also
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be transported by wind or water fowl to other water bodies and thus colonize new habitats.
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In the deeper parts of lakes, these diapausing eggs do not get a hatching stimulus and can
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remain in the sediment providing an unbiased archive of past populations. Ephippia can
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be extracted from sediment cores and either hatched for experimental purposes or directly
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analyzed with molecular genetic methods.12 Analysis of the genetic architecture of
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ephippia revealed that lake eutrophication was associated with a shift in species
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composition and the population structure of evolutionary lineages.10 However, whether
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the shift in species composition was directly caused by phosphate or if phosphate
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concentrations are only a proxy for other parameters like chemical contamination is not
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known. Chemical contaminants can affect natural Daphnia populations either by direct
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toxin uptake, or by indirect ingestion of contaminated algae. Pollutants may
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bioaccumulate in their resting eggs already in the water column or after sedimentation,
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influencing the fitness and their sexual reproduction, and therefore the evolutionary
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potential of an aquatic key species. However, there is almost no information about
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bioconcentration in ephippia in literature. Wyn et al.13 evaluated the temporal and spatial
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patterns of metal contamination in resting eggs from sediment cores. Analysis of organic
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contaminants in ephippia extracted from sediment cores has never been done due to the
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small number of ephippia available in the sediment extraction and the amount needed for
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the chemical analysis.
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Therefore, the objectives of this study were to: (i) clarify to what extent organic
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contaminants can bioconcentrate in Daphnia resting eggs (ephippia) in uptake and
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elimination experiments; and (ii) reconstruct their contamination in the past based on
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sediment concentrations using an equilibrium partitioning model. The information
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obtained from the characterization of Lake Greifensee from our previous work was used
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to select a range of relevant organic contaminants which was complemented with further
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compounds with different hydrophobicity.
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Experimental Section
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Details on the sources, preparation, and storage of reference standards and reagents are
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provided in the Supporting Information (SI). 3 ACS Paragon Plus Environment
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Sample Collection and Preservation
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Two sediment cores were taken from Lake Greifensee, located 11 km to the northeast of
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Zurich, Switzerland. Sediment cores were collected using a free fall gravity corer and
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stored vertically in the dark at 4°C until analysis. Dating of the sediment cores was
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performed by counting yearly laminations as has been described elsewhere.6 Total
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phosphorus concentrations for each sediment layer were measured using peroxodisulfate
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oxidation as described by Ebina et al.14
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Ephippia from the Daphnia longispina-galeata species complex were collected with nets
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from Lake Greifensee during peaks of sexual reproduction in spring and fall 2011.
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Ephippia were stored in 10 L polyethylene (HD-PE) plastic containers (Hünersdorff
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GmbH, Germany) and kept at 12°C before cleaning. Ephippia were cleaned using
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different sieves (mesh sizes:
