Trophodynamics of Organic Pollutants in Pelagic and Benthic Food

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Trophodynamics of organic pollutants in pelagic and benthic food webs of Lake Dianchi: Importance of ingested sediment as uptake route Senrong Fan, Beili Wang, Hang Liu, Shixiong Gao, Tong Li, Shuran Wang, Yong Liu, Xueqin Liu, and Yi Wan Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b03681 • Publication Date (Web): 21 Nov 2017 Downloaded from http://pubs.acs.org on November 21, 2017

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Environmental Science & Technology

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Trophodynamics of organic pollutants in pelagic and benthic food webs of Lake

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Dianchi: Importance of ingested sediment as uptake route

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Senrong Fan1, Beili Wang1, Hang Liu1, Shixiong Gao1, Tong Li1, Shuran Wang3,

4

Yong Liu2, Xueqin Liu3, Yi Wan*1

5 6 7 8 9 10

1

Laboratory for Earth Surface Processes, College of Urban and Environmental Sciences,

Peking University, Beijing 100871, China 2

Key Laboratory of Water and Sediment Sciences Ministry of Education, College of

Environmental Science and Engineering, Peking University, Beijing 100871, China 3

State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology,

Chinese Academy of Sciences, Wuhan, 430072, China

11 12 13 14 15

(Received

)

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*Address for Correspondence:

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Dr. Yi WAN

18

College of Urban and Environmental Sciences

19

Peking University

20

Beijing 100871, China

21

TEL & FAX: 86-10-62759126

22

Email: [email protected] 1 ACS Paragon Plus Environment


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Abstract

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Habitat is of great importance in determining the trophic transfer of pollutants in

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freshwater ecosystems; however, the major factors influencing chemical trophodynamics in

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pelagic and benthic food webs remain unclear. This study investigated the levels of

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p,pʹ-dichlorodiphenyldichloroethylene (p,pʹ-DDE), polycyclic aromatic hydrocarbons (PAHs),

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and substituted PAHs (s-PAHs) in two plankton species, six invertebrate species, and ten fish

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species collected from Lake Dianchi in southern China. Relatively high concentrations of

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PAHs and s-PAHs were detected with total concentrations of 11.4–1400 ng/g wet weight

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(ww) and 5.3–115 ng/g ww, respectively. Stable isotope analysis and stomach content

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analysis were applied to quantitatively determine the trophic level of individual organisms

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and discriminate between pelagic and benthic pathways, and the trophodynamics of the

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detected compounds in the two food webs were assessed. P,pʹ-DDE was found to exhibit

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relatively higher trophic magnification rate in the pelagic food web than in the benthic food

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web. In contrast, PAHs and s-PAHs exhibited greater dilution rates along the trophic levels in

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the pelagic food web. The lower species differences of pollutants accumulated in benthic

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organisms compared to pelagic organisms is attributable to extra uptake via ingested

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sediment in benthos. The average uptake proportions of PAHs and s-PAHs via ingested

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sediment in benthic biotas were estimated to be 31–77%, and that of p,pʹ-DDE was 46%. The

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uptake routes are of importance for assessing the trophic magnification potentials of organic

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pollutants, especially in eutrophic freshwater ecosystems.

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Keywords: Trophodynamics; Substituted PAHs; Benthos; Uptake route; Freshwater

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ecosystem. 2 ACS Paragon Plus Environment

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Introduction

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Environmental pollutants can accumulate to hazardous levels in high-trophic-level

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organisms through food webs and subsequently cause adverse health effects in fish, wildlife,

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and humans.1–3 The trophic transfer of pollutants in food web is an important criterion for

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assessing the potential ecological risks. Although organisms have generally been classified to

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an entire food web based on stable isotope analysis, significantly different trophic transfer

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rates of lipophilic pollutants have been observed for homeotherms and poikilotherms due to

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the different energy requirements and biotransformation abilities between the two groups of

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organisms.4 The mammalian food web also exhibited higher trophic magnification potentials

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for hydrophobic organic substances than the piscivorous food web.5 Therefore, the

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components of food webs are of great importance for accurately assessing the trophic transfer

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of pollutants.

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Influences of food web components on the trophodynamics of pollutants have been

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reported within the marine ecosystems possibly due to relatively high average links per

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species and chain lengths.4,5,6 In comparison, habitat is another important factor in

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determining the trophodynamics of pollutants in freshwater ecosystems.7–9 Kidd et al. found

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that dichlorodiphenyltrichloroethane (DDT) exhibited higher trophic transfer rates in the

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pelagic food web than in the benthic food web in Lake Malawi.7 The possible reason was

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attributed to the relatively low carbon turnover rate at the base of the pelagic food web, which

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increased the accumulation rates of DDT in pelagic consumers occupying high trophic

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levels.7 But the concentrations of methyl mercury (MeHg) and polychlorinated biphenyls

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(PCBs) for high-trophic-level organisms were not found to be significantly different between 3 ACS Paragon Plus Environment


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the pelagic and benthic food webs, while significantly high transfer rates in the pelagic food

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web were also observed for the pollutants in the Yellow Sea and Gulf of St. Lawrence.8-9 The

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trophodynamic discrepancy was then explained by the high energy transfer of pelagic

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organisms.8-9 Based on the above reported mechanisms, compounds undergoing trophic

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dilution or trophic magnification in freshwater ecosystems would both be transferred more

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efficiently to organisms at the top trophic levels in the pelagic food web compared to the

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benthic food web. However, the trophodynamics of compounds undergoing trophic dilution in

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pelagic and benthic food webs remain unknown. The investigation of compounds that

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undergo trophic dilution would help to clarify the major factors influencing the different

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trophodynamics between the two food webs.

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Polycyclic aromatic hydrocarbons (PAHs) are a group of compounds that undergo

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significant trophic dilution in aquatic ecosystems, which has been demonstrated in food webs

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from Bohai Bay and Tokyo Bay.10, 11 Besides PAHs, substituted PAHs (s-PAHs), such as

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oxy-PAHs, nitro-PAHs, and sulfur-PAHs, were also found to be ubiquitous in the

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environment due to their widespread emission sources, the reaction of PAHs with

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atmospheric components, and the transformation of PAHs in sediment and soil.12-15 Most

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studies have focused on their occurrence and fate in the environment and no study has yet

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been made available about their occurrence in biotas possibly due to their less lipophilic

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characteristics. However these compounds have been reported to exhibit higher mutagenic

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and carcinogenic potentials than PAHs.16 It is necessary to investigate the levels and trophic

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magnification potentials of these compounds in biological samples.

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Based on the results of previous investigations, bioaccumulation factors (BAFs) of

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biomagnified and diluted compounds (DDTs and PAHs) could be estimated for the pelagic

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and benthic organisms.7, 17, 18 The BAFs of DDTs in pelagic organisms (103.1-106.1) were

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higher than those in benthos (102.9-105.0), but relatively high BAFs of PAHs were found in

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benthos (105.1-105.8) compared to the pelagic biotas (104.4), suggesting that trophic transfer of

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the two groups compounds might be different in the two types of food webs. In this study,

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p,pʹ-DDE, hexachlorobenzene (HCB), PAHs, oxy-PAHs, nitro-PAHs, and sulfur-PAHs were

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analyzed in the aquatic food web of Lake Dianchi. Stable isotope analysis and stomach

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content analysis were applied to quantitatively determine the trophic levels of individual

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organisms and discriminate between pelagic and benthic pathways. The trophic transfer of

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detected pollutants in the pelagic and benthic food webs was assessed, and the potential

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mechanisms influencing the trophodynamics of pollutants in the two types of food webs were

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clarified. The results facilitate better understanding of the variability in contaminant

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trophodynamics driven by ecological processes (i.e. pelagic vs benthic food webs).

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Materials and Methods

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Chemicals and Reagents

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The target chemicals consisted of p,pʹ-DDE, HCB, 16 PAHs (naphthalene (Na),

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acenaphthylene (Acy), acenaphthene (Ace), fluorene (FE), phenanthrene (Ph), anthracene

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(An), fluoranthene (Fl), pyrene (Py), chrysene (Ch), benz[a]anthracene (BaA), benzo-

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[b]fluoranthene

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indeno[1,2,3-cd]pyrene (IP), benzo[ghi]perylene (BP) and dibenz[a,h]anthracene (DA)) and

(BbF),

benzo[k]fluoranthene

(BkF),


benzo[a]pyrene

(BaP),


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14 s-PAHs (dibenzothiophene (DBT), dibenzyl sulfide (DS), benzophenone (BPH),

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9-fluorenone (9-Fl)，benzothiophene (BT), anthrone (AnT), anthraquinone (AT), diphenyl

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disulfide (DD), 2-naphthalenethiol (2-NT), thianthrene (TT), 3-nitrophenanthrene

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(3-NPh), 9-nitroanthracene (9-NAn), 3-nitrofluoranthene (3-NFl), 1-nitropyrene (1-NPy)).

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The standards and surrogate standards (PCB 121, acenaphthene-d10, phenanthrene-d10,

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chrysene-d12, and perylene-d14) were obtained from AccuStandard (New Haven, CT).

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Certified reference material GBW(E)100130 (freeze-dried muscle of sea bass) was purchase

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from National Institute of Metrology, China, and standard reference material 2974a

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(freeze-dried mussel tissue) was supplied by National Institute of Standards and Technology

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(Gaithersburg, MD, USA). All solvents (dichloromethane, acetonitrile, acetone and hexane)

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were HPLC grade purchased from Fisher Scientific (NJ). Sodium sulfate and aluminum oxide

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were analytical grade and were heated at 400°C for 4 h before use.

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Sample Collection

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Lake Dianchi is a typical shallow plateau lake located in the southwest region of China

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with an altitude of 1886 m, an area of about 300 km2, and an average depth of approximately

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4.7 m.19 The major components of the Lake Dianchi food web were collected in August 2015,

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including two planktons species (phytoplankton and seston), six invertebrate species (clam

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(Anodonta woodianawoodiana), gastropods (Cipangopaludina cahayensis, Bellamya

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quadrata), shrimps (Neocaridina denticulate, Macrobrachium nipponense),

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(Palinuridae)), ten fish species (catfish (Silurus asotus), goby (Neogobius melanostomus),

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common carp (Cyprinus carpio), yellow catfish (Pelteobagrus fulvidraco), silvery white fish

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(Anabarilius alburnops), crucian carp(Carassius auratus), silver carp (Hypophthalmichthys 6 ACS Paragon Plus Environment

and crayfish

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molitrix), redfin culter (Cultrichthys erythropterus), whitebait (Hemisalanx prognathus Regan)

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and needle fish (Tylosurus melanotus)).

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The phytoplankton and seston samples were obtained by horizontal surface tows using a

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0.5 m i.d by 2 m long net (250 µm mesh) and a 0.5 m i.d by 1 m long net (125 µm mesh),

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respectively, from three locations (24°50ʹ46ʺN, 102°44ʹ16ʺE; 24°50ʹ40ʺN, 102°41ʹ34ʺE;

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24°49ʹ6ʺN, 102°43ʹ5ʺE). Phytoplankton samples mainly consisted of microcystis, and seston

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samples consisted of zooplankton (cladocerans and copepods) and microcystis. Invertebrates

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and fish were obtained by bottom trawling. All of the samples were stored at −20 °C in amber

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vials prior to analysis. The details of chemical analysis were provided in the Supporting

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Information (SI), Table S1, S2, S3 and S4.

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Stable Nitrogen and Carbon Isotope Analysis

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The lipid-deprived samples were dried at 80 °C for about 4 h. Subsequently, exactly 0.3

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mg of each sample was set in a Sn capsule (containing no air) and combusted at 1000–1050

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°C to convert the nitrogen and carbon into N2 and CO2, which were carried by dried and

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column-cleaned helium gas, separated on a gas chromatography column (Porapak QS), and

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analyzed using a mass spectrometer (Thermo Delta Plus, Finnigan MAT) equipped with an

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interface (ConFlo III, Finnigan MAT). Stable isotope values were expressed as follows:

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δ15N = ((15N / 14Nsample / 15N / 14Nstandard) − 1) × 1000 (‰)

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δ13C = ((13C / 12Csample /13C / 12Cstandard) − 1) × 1000 (‰)

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The

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N/14Nstandard and

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C/12Cstandard values were based on atmospheric N2 (air) and Pee

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Dee belemnite (PDB), respectively.

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Stomach Content Analysis 7 ACS Paragon Plus Environment


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Stomach contents of the collected species except for phytoplankton and seston were

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analyzed. The stomach content analysis was conducted following a method reported

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previously.20 Samples used for stomach content analysis were delivered in an ice-chilled box

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to the local laboratory. The full stomachs were removed, cut open, and the stomach contents

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were preserved in 10% formalin. The contents were examined microscopically, sorted and

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identified with the aid of identification atlases. After identification, prey items were classified

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into pelagic and benthic groups.

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Data Analysis

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As the trophic magnification factor (TMF) reflects the average increasing amount per

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trophic level rather than specific prey–predator relationships, an increasing number of studies

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have reported trophic transfer of pollutants using the TMF by correlating the concentration of

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pollutants in organisms and trophic level. In this study, trophic levels were estimated based on

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stable isotopes of individual organisms by equation (1).

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TLsample = 1.5 + (δ15Nsample – δ15Nbasal) /3.77

(1)

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where TL and δ15N represent the trophic levels and the stable nitrogen values of individual

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organisms. TL of the pelagic organisms were estimated by assuming that seston represents a

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basal trophic level of 1.5, since seston is determined to be composed of phytoplankton and

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mesozooplankton.21 In the benthic food web, trophic levels were determined relative to

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crayfish, which was assumed to occupy a basal trophic level of 2.0, since crayfish

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(Palinuridae) has been reported to substantially feed on detritus and periphytic algae which

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occupied a trophic level of 1.0 in Lake Dianchi.22-23 The diet–tissue discrimination factor

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associated with trophic transfer was set as 3.77 based on the prey–predator relationship 8 ACS Paragon Plus Environment

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between silver carp (Hypophthalmichthys molitrix) and seston reported previously in Lake

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Dianchi.22 The TMFs were calculated by the following equations based on the relationship

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between trophic level and logarithmic concentrations of individual organisms.24 Log Concentration (lipid-normalized) = a + b × TL

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(2)

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where a and b are the intercept and slope of the single linear regression, respectively. The

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TMF was calculated using the slope b by the following equation: TMF = 10b

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(3)

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Pearson’s rank correlation test was used to examine the relationship between trophic level

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and logarithmic concentrations of pollutant. If the p value was below 0.05, the regression was

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supposed to be significant. In the case of nondetected (ND) concentrations, various

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percentages of MDLs assigned to the ND sample were tested, and no significantly different

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results were obtained for the liner regression analysis. Similar to the previous investigations,4,

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10, 25

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more than 40% of samples were below the MDLs (HCB, Na, Acy, Ace, BT, AnT, AT, DD,

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2-NT, TT, 3-NPh, 9-Nan, 3-NFl and 1-Npy), the chemicals were not included in the

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calculations of TMFs. For all of the tests, the SPSS 19.0 software was used (SPSS Inc.,

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Chicago, IL, USA).

concentrations below the detection limit were set as half of the MDL. In this study, when

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Results and Discussion

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Trophic Structures of Benthic and Pelagic Food Webs

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The results of stomach content analysis and previously reported habitats were applied to

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assign species to either the “pelagic” or “benthic” food webs. The phytoplankton and seston 9 ACS Paragon Plus Environment


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were considered as the basal food sources for the pelagic food web.26 For the invertebrates,

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stomach content analysis showed that the diet of shrimp (Neocaridina denticulata) mainly

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consisted of planktons, which was consistent with the observation that this species mainly fed

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on algae and zooplankton.27 The larvae of shrimp (Macrobrachium nipponense) principally

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fed on zooplankton and the juvenile organisms exhibited nocturnal swimming activity to take

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advantage of pelagic food sources.28 Thus, both of the shrimp species belonged to the pelagic

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food web. The preferred habitat of crayfish lay adjacent to the sedimentary bottoms,29 clams

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generally obtained organic matter and phosphate from the sediment by direct ingestion or by

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feeding on bacteria associated with these materials,30 gastropod (Cipangopaludina cahayensis)

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commonly inhabited muddy sites and exhibited intense feeding activities on the upper layer

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of sediment,31 and gastropod (Bellamya quadrata) was a common component of the benthic

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community in lakes.32-33 Hence, these four species were assigned to the benthic food web. For

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fishes, the stomach content analysis showed that the most frequent diet of silver carp

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consisted of phytoplankton and zooplankton, and that of whitebait consisted of zooplankton

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(cladocerans and copepods). This was consistent with the fact that these two species were

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planktivores.26 Similarly, the crucian carp also showed a planktivorous dietary habit.34 It has

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been reported that needlefish, silvery white fish, and redfin culter were all components of

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pelagic communities.35 Thus, these six fish species belonged to the pelagic food web. Based

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on the stomach content analysis, chironomidae, occupying the trophic level of about 2,22, 36 is

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one of the components in the diet of goby, catfish, yellow catfish, and common carp. Besides

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chironomidae, diet of common carp comprised of about 50% crustaceans (i.e. shrimp), that of

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yellow catfish comprised of about 65% invertebrates and fishes, that of goby contained 70% 10 ACS Paragon Plus Environment

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benthic invertebrates (i.e. mudsnail), and that of catfish had 10% detritus. Similar to the

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previous publications, catfish and yellow catfish have been reported to exhibit benthivorous

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dietary habits,26 common carp mainly consumed benthic organisms,37 and goby mainly

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consumed zebra mussels (a benthic dwelling mollusk).38 Therefore, catfish, yellow catfish,

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common carp, and goby were assigned to the benthic food web. Overall, the pelagic food web

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consisted of ten species, while the benthic one consisted of eight species. The details of the

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various species in each food web are shown in Table 1 and S4.

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Stable carbon isotopes were applied to discriminate between pelagic and benthic energy

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pathways in the food webs, as different energy sources have distinct δ13C values.39-40 The

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δ13C values ranged from −27.8‰ to −14.8‰ in the benthic food web and from −16.6‰ to

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−14‰ in the pelagic food web (Table S5, Figure 1). Significantly higher values of δ13C were

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observed in pelagic organisms compared with benthic organisms (p=0.008). These

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differences could be explained by the fact that pelagic grazing rates were significantly higher

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than benthic grazing rates in the eutrophic Lake Dianchi, and the high grazing rates and low

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photosynthetic fractionation resulted in an enrichment of δ13C in pelagic organisms.41-42

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Nitrogen isotope analysis was used as an indicator of trophic level.43 The δ15N values

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ranged from 12.9‰ to 23.9‰ in the benthic food web and from 17.6‰ to 24.4‰ in the

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pelagic food web (Table S5, Figure 1). The estimated trophic levels were 1.10±0.07–

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4.02±0.07 and 1.41±0.03–3.19±0.05 for the benthic and pelagic food webs, respectively. The

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trophic levels obtained in this study are consistent with previous reports that used traditional

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stomach content analysis. Specifically, as shown in Table 1, the plankton species

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(phytoplankton and seston) occupied the trophic level of 1.41–1.5, which was located 11 ACS Paragon Plus Environment


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between the trophic levels of phytoplankton (1.00) and zooplankton (2.00–2.04) reported

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previously for Lake Dianchi.22 The pelagic fish represented the trophic level of 2.16–3.19,

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which is comparable to that reported for similar fish species (2.00–3.55) in Lake Dianchi.22

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The trophic levels in this study were also consistent with the previously reported prey–

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predator relationships.44 For example, the silver carp mainly fed on planktons, and there was

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approximately one order of magnitude between their calculated trophic levels.

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Trophodynamics in Benthic and Pelagic Food Webs

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Various organic pollutants, such as p,pʹ-DDE, HCB, PCBs, Poly Brominated Diphenyl

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Ethers (PBDEs), PAHs, and s-PAHs, were investigated in the biota samples in Lake Dianchi,

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and only p,pʹ-DDE, PAHs, and s-PAHs were detected with relatively high concentrations.

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Sedimentary records of DDTs and PAHs in Lake Dianchi have reported that DDTs stemmed

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primarily from historical usages of the chemical, and PAHs originated mainly from domestic

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combustion of coal and biomass.45 The relatively high concentrations of PAHs in the area

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were due to the limited water exchange and high sediment TOC contents in Lake Dianchi,

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which favored the sequestrations of PAHs in the aquatic environment.45-46 The concentrations

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of p,pʹ-DDE, PAHs, and s-PAHs in the pelagic and benthic food webs are shown in Table 1.

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Whereas the concentrations of p,pʹ-DDE in organisms (ND–550 ng/g lipid weight (lw)) in

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Lake Dianchi were comparable to those reported for biological samples obtained from other

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lakes (6.8–368.8 ng/g lw; 7.2–295 ng/g lw; 75.4–838 ng/g lw),7, 47, 48 high concentrations of

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PAHs (1300–4200 ng/g lw) were observed in the fish from Lake Dianchi compared with

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those from Bohai Bay (43–247 ng/g lw), Tokyo Bay (806.7 ng/g lw), or Taihu Lake (median:

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351–1380 ng/g lw).10, 11, 48 To the best of our knowledge, this is the first report concerning 12 ACS Paragon Plus Environment

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s-PAHs in aquatic organisms, and BPH, 9-Fl, DBT and DS exhibited high detection

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frequencies (>60%) across all of the samples. The total concentrations of the four s-PAHs

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were 8.1–114, 44.0–96.4 and 5.3–91.5 ng/g wet weight (ww) in planktons, invertebrates, and

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fish, respectively. Of the detected s-PAHs, BPH was the predominant compound in all

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samples, representing 33–88% of the total concentration of s-PAHs, followed by 9-Fl (9–

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40%), DBT (4–19%), and DS (3–12%). When compared to the PAHs, the concentration

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ratios between PAHs and s-PAHs were 0.01–0.4 for the planktons and invertebrates, and

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0.44–1.3 for most of the fish species.

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A significant positive statistical linear regression was obtained between the logarithmic

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lipid-based concentrations of p,pʹ-DDE and the trophic levels for both the pelagic and benthic

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food webs, and the TMFs of p,pʹ-DDE were 4.41 and 2.03 for the pelagic and benthic food

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webs, respectively (Table 2). This result is consistent with the observations of numerous

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reports in the literature for lake ecosystems.4, 25, 47–49 The observed trophic magnification of

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p,pʹ-DDE supported that the pelagic and benthic food webs studied were appropriate to test

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the trophodynamics of pollutants. p,pʹ-DDE exhibited higher trophic transfer rate through the

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pelagic food web (slope=0.64) than through the benthic food web (slope=0.31, Figure 2).

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Significantly higher transfer rates in the pelagic food web were also observed for DDTs,

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chlordane, PCBs, and MeHg in previous studies.7–9 Kidd et al. found that the concentrations

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of DDT in pelagic fish were significantly higher than those in benthic fish occupying

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comparable trophic levels, and the possible reason for this could be that relatively low carbon

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turnover rate at the base of the pelagic food web, which increased the accumulation rates of

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DDT in pelagic consumers occupying high trophic levels.7 However, no significantly 13 ACS Paragon Plus Environment


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different concentrations of MeHg and PCBs were found for high-trophic-level organisms

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between the pelagic and benthic food webs, while significantly higher trophic magnification

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slopes were observed for these pollutants in the pelagic food web compared with the benthic

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food web.8, 9 This trophodynamic discrepancy could be due to the inter-taxa differences in

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energy requirements, and trophic transfer would be more efficient as a result of more linear

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energy transfer through the pelagic food web compared to the more reticulate benthic food

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web.8, 50

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Whereas most studies concerning the trophodynamics of pollutants in the benthic and

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pelagic food webs have focused on compounds exhibiting significant trophic magnification,

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the fates of compounds undergoing trophic dilution in the two types of food webs remain

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unknown. In this study, extremely high concentrations of predominant PAHs (21-32 µg/g lw)

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and s-PAHs (4.6-10 µg/g lw) based on lipid weight were detected in phytoplankton and

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seston (Table 1), and similar high concentration of PAHs were also observed in seson

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collected from northern Blatic (∑PAHs: 28 µg/g lw)51 and planktons from Mediterranean Sea,

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Black Sea and Marmara Sea (∑PAHs estimated to be 6-37 µg/g lw)52. The possible reason

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could be that the plankton can accumulate PAHs through passive physicochemical adsorption

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and active absorption, leading to the high levels in the organisms.53 Thus the two organisms

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were not included in the trophodynamic analysis of PAHs and s-PAHs in the food web. The

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PAHs and s-PAHs, including FE, An, BPH, 9-Fl, and DS, were detected with frequencies

305

higher than 60% in all samples and their trophodynamics were assessed. A statistical

306

regression analysis was conducted between the trophic levels and the logarithmic lipid-based

307

concentrations of PAHs and s-PAHs. Significant negative correlations were observed 14 ACS Paragon Plus Environment

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308

between the trophic levels and the lipid-equivalent concentrations of FE, An, and BPH in the

309

pelagic food web with TMF values ranging from 0.36 to 0.5, and no significant corrleations

310

were found for 9-Fl and DS (TMFs: 0.48-0.58). In the benthic food web, the PAHs

311

underwent significant trophic dilution with TMFs of 0.72–0.85, and no significant

312

correlations were obtained for the s-PAHs (TMF: 0.65–0.86, Figures 3 and 4, Table 2). It

313

should be noted that the TMF values of assessed PAHs and s-PAHs in the pelagic food web

314

were significantly lower than those in the benthic food web (paired t-test, t=4.938, p=0.008,

315

Table 2). Trophic dilution of PAHs in aquatic food web were largely attributed to the

316

efficient metabolic transformation in animals at higher trophic levels, since cytochromes

317

P450, which can catalyze the oxidation of various chemicals, are relatively rich in

318

vertebrates.10 The pelagic and benthic food web both have invertebrates and vertebrates

319

occupying similar trophic levels, thus the specie differences would not result in the different

320

trophodynamics between the two types of food webs. It is expected that organisms in pelagic

321

food webs would exhibit high accumulation and energy transfer rates for various organic

322

pollutants,7, 54 but based on the mechanisms PAHs would be transferred more efficiently to

323

organisms at the upper trophic levels in pelagic food webs compared to benthic food webs,

324

resulting in relatively high TMF values for PAHs in pelagic food webs. However, this rule

325

seems to contradict the observations of PAHs in this study (Table 2), suggesting the existence

326

of other mechanisms that drove the difference of trophic transfer between the pelagic and

327

benthic food webs.

328

Ingested Sediment versus Diet as Uptake Routes



329

Deposit-feeding organisms can take up organic contaminants through various routes,

330

such as diet, and sediment ingestion.55-56 It has been reported that various pollutants are able

331

to accumulate in benthos through ingested sediment (such as oligochaete, copepod, mussel,

332

and fish), and the uptake of hydrophobic pollutants takes place manly through the

333

ingestion.55-60 In pelagic food webs, organisms accumulate organic pollutants mainly through

334

dietary uptake, and the trophic transfer of compounds in the food web is a reflection of prey–

335

predator accumulation. In comparison, the extra uptake via ingested sediment in benthos

336

would reduce the concentration differences of pollutants among species, thus resulting in the

337

relatively flat trend of correlations between trophic level and contaminant concentrations in

338

the benthic food web (Figure 5). In this study, the differences of trophic transfer between

339

pelagic and benthic food webs were applied to estimate the contribution of ingested sediment

340

as an uptake route in benthos by the following equations.

341

log C1 = a1 + b1 × TL

(4)

342

Equation (4) shows the linear regression between logarithmic pollutant concentrations and

343

trophic levels in the pelagic food web. C1 and TL represent the pollutant concentrations and

344

trophic levels of the organisms, respectively. Pelagic organisms accumulate pollutants mainly

345

through dietary uptake, which is supported by the fact that the δ13C values were similar for the

346

pelagic organisms, suggesting that they consumed the same pelagic carbon sources.40

347

log C2 = a2 + b2 × TL

(5)

348

Equation (5) shows the linear regression between the trophic levels and total logarithmic

349

concentrations of pollutants in the benthic food web. C2 represents the concentrations of

350

pollutants in benthic organisms. 16 ACS Paragon Plus Environment

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351


log (C2 − ∆) = a3 + b1 × TL

(6)

352

Equation (6) shows the linear regression between trophic levels and logarithmic

353

concentrations of pollutants contributed from dietary uptake in benthic organisms. ∆

354

represents the average uptake concentrations of pollutants via ingested sediment in the

355

benthic food web. “C2 − ∆” represents the pollutant concentrations in biota contributed

356

through dietary uptake. This equation shows the dietary accumulation of pollutants in the

357

benthic food web. Similar transfer efficiencies of dietary accumulation have been reported for

358

benthic (TE=4.9%) and pelagic (TE=5.1%) food webs.22 Thus, the accumulation of pollutants

359

through diet was similar for the pelagic and benthic food webs, and b1 was used in this

360

equation. According to Equation (6), a regression was generated between “C2 − ∆” and TL,

361

and the slope of the regression was fitted to b1. In the calculations, C2, TL and b1 were known

362

variables, and the ∆ value was estimated using the least-squares method by optimizing the

363

slope of the linear statistical regression to b1. The contribution of ingested sediment

364

accumulation to the total body burden of pollutants in the benthos (Psediment, %) was

365

calculated using Equation (7).

366

Psediment = ∆ / C2 × 100

(7)

367

Based on the above equations and the concentrations obtained in this study, the average

368

Psediment for p,pʹ-DDE in benthos was estimated to be 46±34%, and Psediment was in the range

369

of 48-79% and 7-39% in the benthic gastropods and fish, respectively. The Psediment of

370

p,pʹ-DDE can be estimated in previous studies about sediment exposed mussels (D. bugensis,

371

52±22%)60 and benthic marine fish (Pleuronectes yokohamae, 39%)61, and the reported

372

proportions of p,pʹ-DDE were within the estimated ranges obtained in this study. It should be 17 ACS Paragon Plus Environment


373

noted that relatively high Psediment values of p,pʹ-DDE in gastropods compared with fish were

374

found in the results of both the previous exposure experiments and present estimations. The

375

values of Psediment for FE, An, BPH, 9-Fl, and DS were estimated to be 68±15%, 59±22%,

376

65±17%, 77±19% and 31±15%, respectively. The contribution proportions of PAHs in this

377

study (59-77%) were slightly lower than those reported in PAH-exposed gastropods (89–

378

99%).62 The similar values suggested that the method described above was appropriate for

379

estimating the ingested-sediment accumulation of organic compounds in benthic food webs,

380

and sediment uptake is an important route for pollutants accumulated in benthos. We also

381

applied this method to calculate the contribution of ingested-sediment accumulation for

382

MeHg based on results obtained in a previous report,8 and the Psediment value for MeHg was

383

estimated to be 35±34%. It is interesting to note that the Psediment values of p,pʹ-DDE and

384

MeHg (35–46%) were lower than those for PAHs (59–77%). The possible mechanism

385

underlying this difference could be that PAHs is more difficultly assimilated than other

386

hydrophobic compounds (e.g. MeHg, p,pʹ-DDE);62 hence, the accumulation of PAHs and

387

s-PAHs relies more on sediment uptake.

388

Previous studies about the trophic transfer of organic pollutants have generally explored

389

the trophodynamics of pollutants in the entire food web, including both benthic and pelagic

390

organisms.48, 49, 64, 65 In this study, significant statistical regressions were obtained for the

391

whole-lake food web between the trophic level and logarithmic lipid-normalized

392

concentrations of the highly detected pollutants except 9-Fl (Figure S1-S2, Table 2). Large

393

differences were observed for the TMFs of the whole-lake food web compared with those of

394

the individual pelagic or benthic food web (Table 2). For example, the TMFs of An and FE in 18 ACS Paragon Plus Environment

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395

the whole-lake food web were lower than that in the benthic food web but higher than that in

396

the pelagic food web (Table 2). We noticed that the significantly different TMFs between

397

pelagic and benthic food webs were all reported for eutrophic freshwater ecosystems.7–9, 66 It

398

has been reported that the suspension feeding rates of pelagic organisms are higher than those

399

of benthos, and the differences increased with increasing concentrations of chlorophyll a.42

400

Thus, the dietary uptake of the benthos became low in the eutrophic ecosystem, resulting in

401

the high contributions of ingested sediment as an uptake route, and subsequently different

402

trophodynamics of the pollutants.

403

In conclusion, p,pʹ-DDE and PAH compounds showed different trophodynamics

404

between the pelagic and benthic food webs of Lake Dianchi. The concentrations of all

405

pollutants exhibited lower species differences in the benthic organisms compared to the

406

pelagic organisms as a consequence of the extra uptake via ingested sediment in the benthos.

407

The estimated uptake proportions via sediment for PAHs and s-PAHs were higher than those

408

of p,pʹ-DDE and MeHg. Large habitat differences between pelagic and benthic organisms in

409

eutrophic lakes would result in the different trophodynamics of pollutants in the two types of

410

food webs.

411 412

Acknowledgments

413

The research is supported by National Basic Research Program of China

414

(2015CB458900) and National Natural Science Foundation of China (21422701,

415

201677003).

416 417

Supplementary Data 19 ACS Paragon Plus Environment


418

Text, figures, and tables addressing: (1) chemical analysis of biota samples; (2)

419

trophodynamics of target pollutants in the whole food web in Lake Dianchi; (3) internal

420

calibrations of individual chemicals; (4) spiked amounts, method detection limits, recovery

421

rates and quantification accuracies of individual chemicals; (5) concentrations of PAHs in

422

certified reference materials; (6) mean biological parameters and δ13C and δ15N values in

423

pelagic and benthic food webs.


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622 623

Page 26 of 34

Table 1. Mean biological parameters and concentrations (ng/g wet weight) of p,pʹ-DDE, PAHs, and s-PAHs in the pelagic and benthic food webs of Lake Dianchi, China. Species

a

Sample Length (cm) Weight (g) numbers

TL

p,p' -DDE

FE

An

BPH

9-Fl

DBT

DS

Pelagic food web b

—

—

1.41±0.03

b

CA AA Ce HP TM

2 6 6 6 6 6 6 6 6 6

— 4.44±0.56 8.62±0.77 6.58±0.63 6.58±0.63 13.6±0.97 7.66±0.95 14.1±1.17 10.2±0.56 10.4±1.08

— 0.58±0.19 22.0±6.05 3.02±0.87 3.02±0.87 77.6±17.5 5.24±2.37 29.7±7.46 1.50±0.44 4.06±0.69

1.50±0.22 1.56±0.08 2.16±0.10 2.18±0.03 2.50±0.14 2.74±0.03 2.89±0.05 3.08±0.04 3.17±0.08 3.19±0.05

AW CC BQ Pa SA CCS CCO PF

6 6 6 6 6 6 6 6

7.29±1.11 4.48±0.43 4.50±0.39 8.58±3.14 8.62±0.77 4.56±0.33 6.20±0.40 9.18±3.34

40.8±19.9 17.0±5.27 15.5±5.09 6.64±2.43 22.0±6.05 1.64±0.43 5.60±0.95 24.7±30.3

1.10±0.07 1.22±0.06 1.29±0.12 2.00±0.11 2.63±0.19 3.18±0.03 3.53±0.02 4.02±0.07

PP Se Nd 1

CA MN HY

2

624 625 626

2

ND

74.0±5.11 6.80±2.02 58.1±21.4 28.7±8.82 19.0±6.98 8.92±2.34

ND 13.3±1.47 0.81±0.42 68.6±58.0 1.64±0.46 20.6±3.33 1.02±0.38 20.5±17.3 3.04±1.39 30.7±5.48 0.76±0.83 8.44±3.81 3.48±1.71 18.1±9.89 3.07±1.12 10.7±4.79 5.16±1.05 25.3±12.7 4.48±0.91 23.0±13.9 Benthic food web 0.47±0.06 15.9±2.28 0.75±0.30 13.4±7.62 0.83±0.76 24.0±4.36 0.48±0.20 18.5±7.78 2.95±0.59 14.2±7.97 2.12±0.89 30.1±10.8 5.20±0.22 21.8±7.04 12.3±3.33 19.5±10.0

3.08±0.77 9.80±8.73 1.26±0.48 3.97±2.97 1.72±0.42 ND 1.40±0.59 ND 2.87±1.41 4.51±1.74

4.44±2.14 61.5±34.4 30.9±2.85 43.2±18.2 24.8±3.10 ND 35.6±3.85 10.2±7.52 36.5±6.73 69.8±4.22

1.67±0.90 20.8±20.9 3.63±2.13 6.99±5.79 ND ND 6.86±2.04 ND 8.26±2.08 13.3±2.66

1.05±0.63 9.93±11.1 ND 3.67±3.47 2.60±0.68 ND ND ND 4.62±1.55 5.16±0.59

0.92±0.71 4.19±3.29 0.98±0.51 1.92±0.59 0.63±0.27 0.45±0.10 1.17±0.54 0.67±0.28 2.88±0.44 3.25±0.58

2.95±0.12 3.09±1.30 3.42±2.12 2.26±1.26 1.99±0.81 3.54±1.95 2.53±1.16 2.39±1.56

38.0±12.5 39.8±2.30 35.6±2.94 36.1±7.67 33.1±5.97 66.3±18.3 36.6±5.66 51.8±11.6

4.52±1.62 7.97±0.59 5.91±2.95 4.42±3.49 4.84±2.06 8.06±5.49 6.39±2.39 8.12±3.15

1.98±0.56 3.08±0.89 ND 2.09±1.38 ND 5.02±3.79 ND 3.01±1.88

3.53±0.90 5.33±1.08 1.48±0.41 1.34±0.46 1.07±0.62 2.23±0.80 1.55±0.76 2.29±0.66

Species: PP = Phytoplankton; Se = Seston; Nd = Shrimp (Neocaridina denticulata); CA1 = Crucian carp (Juvenial) (Carassius auratus); MN= Shrimp (Macrobrachium nipponense); HY = Silver carp (Hypophthalmichthys molitrix); CA2 = Crucian carp (Adult) (Carassius auratus); AA = a

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Page 27 of 34

627 628 629 630 631


Silvery White Fish (Anabarilius alburnops); Ce = Redfin culter (Cultrichthys erythropterus) ; HP = Whitebait (Hemisalanx prognathus Regan); TM = Neddle fish (Tylosurus melanotus); AW = Clam (Anodonta woodiana woodiana); CC = Gastropod (Cipangopaludina cahayensis); BQ = Gastropod (Bellamya quadrata); Pa = Crayfish (Palinuridae); SA = Catfish (Silurus asotus); CCS = Goby (Neogobius melanostomus); CCO = Common carp (Cyprinus carpio); PF = Yellow Catfish (Pelteobagrus fulvidraco). b Each sample was polled samples collected from three sampling locations.

632

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633 634

Table 2. Statistical results of regression analysis between logarithmic concentration and trophic level (slope, p value of slope) and TMFs in the pelagic, benthic, and whole-lake food webs. Compounds p,p'-DDE FE An BPH 9-Fl DS

635

Page 28 of 34

Pelaigc food web

Benthic food web

slope b

r

2

TMF

p

0.64 -0.40 -0.45 -0.30 -0.32 -0.24

0.72 0.65 0.44 0.28 0.20 0.16

4.41 0.40 0.36 0.50 0.48 0.58

0.002 0.015 0.025 0.035 0.058 0.112

Whole-lake food web

slope b

r

2

TMF

p

slope b

r2

TMF

p

0.31 -0.07 -0.14 -0.07 -0.07 -0.18

0.68 0.79 0.91 0.46 0.35 0.45

2.03 0.85 0.72 0.86 0.86 0.65

0.018 0.002 0.001 0.060 0.163 0.096

0.42 -0.14 -0.22 -0.14 -0.14 -0.22

0.58 0.36 0.37 0.18 0.14 0.29

2.63 0.72 0.60 0.72 0.73 0.61

Trophodynamics of Organic Pollutants in Pelagic and Benthic Food

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