Quantifying Bioavailability of Pyrene Associated with Dissolved

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Quantifying Bioavailability of Pyrene Associated with Dissolved Organic Matter of Various Molecular Weights to Daphnia magna Hui Lin, Xinghui Xia, Siqi Bi, Xiaoman Jiang, Haotian Wang, Yawei Zhai, and Wu Wen Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b05520 • Publication Date (Web): 14 Dec 2017 Downloaded from http://pubs.acs.org on December 15, 2017

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Quantifying Bioavailability of Pyrene Associated with Dissolved Organic

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Matter of Various Molecular Weights to Daphnia magna

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Hui Lin, Xinghui Xia*, Siqi Bi, Xiaoman Jiang, Haotian Wang, Yawei Zhai, Wu Wen

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School of Environment, Beijing Normal University, State Key Laboratory of Water Environment Simulation,

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Beijing 100875, China

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Corresponding author. Tel./fax: +86 10 58805314.

E-mail address: [email protected] (X. Xia) 1

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ABSTRACT

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Dissolved organic matter (DOM) is a key environmental factor for the bioavailability of

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hydrophobic organic compounds (HOCs) in natural waters. However, the bioavailability of

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DOM-associated HOCs is not clear. In this research, pyrene was selected as a model HOC and its

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freely dissolved concentration (Cfree) was maintained by passive dosing systems. The

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immobilization and pyrene content in the tissues excluding gut of Daphnia magna were examined

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to quantify the bioavailability of DOM-associated pyrene. The results indicated that DOM

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promoted the bioavailability of pyrene when the Cfree of pyrene was kept constant, and the

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bioavailability of pyrene associated with DOM of various molecular weights was ordered as

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middle molecular weight (5-10K Da) DOM > lower molecular weight ( higher molecular weight (>10K Da) DOM. The influencing mechanisms of

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DOM molecular weight were related with the partition of pyrene between DOM and water, the

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uptake routes of DOM by Daphnia magna, and the desorption or release of pyrene from DOM in

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the gut of Daphnia magna. The findings obtained in this research suggest that the bioavailability

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of DOM-associated HOCs should be taken into account for the eco-environmental risk

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assessment of HOCs in water systems.

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Key words: Bioavailability; Dissolved organic matter (DOM); Molecular weight; Passive dosing

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systems; Immobilization; Freely dissolved concentration

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1. INTRODUCTION

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Hydrophobic organic compounds (HOCs) and their risks to the environment, organisms, and

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human health have aroused wide public concern for a long time. In natural waters, HOCs can be

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easily associated with dissolved organic matter (DOM) by various forms of binding and

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adsorption,1,2 such as hydrogen bonding, covalent bonds, hydrophobic interactions, and

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partitioning.3-8 The ubiquity of DOM in environments and its ability to sorb HOCs exert

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significant influence on the distribution, fate, and bioavailability of HOCs.9-12 For example, the

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distribution, fate, and bioavailability of polycyclic aromatic hydrocarbons (PAHs) are greatly

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influenced by DOM in natural waters.13,14

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Most of previous studies suggested the presence of DOM could decrease the freely dissolved

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HOC concentrations when the total dissolved concentrations of HOCs remain unchanged in water

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due to the binding of HOCs with DOM,15,16 and hence reduce HOC bioavailability and

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toxicity.17-19 For example, Perminova et al.20 found the toxicity of PAHs to Daphnia magna was

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alleviated by humic acids (HA) and fulvic acids (FA), and Yang et al.21 reported DOM at low

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levels (3-20 mg-C L-1) reduced the uptake of cyfluthrin by Daphnia magna. On the contrary, the

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enhancement of PFAS bioaccumulation by Daphnia magna after addition of DOM at a low level

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was found by Xia et al. because the uptake and elimination rates of PFAS in Daphnia magna were

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influenced by DOM.22 In addition, it has been reported that DOM can enhance the diffusive mass

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transfer of PAHs in the unstirred boundary layer, which is often seen as the rate limiting process

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for the PAH uptake in aquatic organisms.23,24 According to Ter Laak et al.,25 when

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benzo[b]fluoranthene was controlled at a low level, its accumulation by Lumbriculus variegatus

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increased after adding 55 mg-C L-1 HA resulting from the DOM-promoted transport of

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benzo[b]fluoranthene to organisms. There is also evidence that phenanthrene biodegradation rates

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were enhanced by adding HA in a saline mineral medium resulting from the HA-mediated

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transport of phenanthrene to the cells.26 Furthermore, previous research revealed microbes could 4

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degrade the DOM-associated HOCs directly.27 Divergent findings above indicate that the

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influence of DOM on the bioavailability of HOCs is not well understood, and the main reason for

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this is that the bioavailability of DOM-associated HOCs is not well studied and quantified.

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Dissolved organic matter is a complex and heterogeneous mixture, and its structural

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components are still elusive due in part to molecular complexity of DOM.28 Because the

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molecular weight of DOM is closely related to its functionality and source, the molecular weight

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distribution of DOM has been extensively investigated in natural waters including streams, lakes,

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rivers, and sea.29-32 Many studies suggest the sorption on and desorption of HOCs from DOM are

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related to DOM molecular weight.33,34 The larger molecular weight of DOM is, the bigger

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organic carbon normalized partition coefficient (Kdoc) of pyrene is.35,36 Furthermore, Xia et al.37

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reported the bioaccumulation of perfluorooctanoic acid by Daphnia magna was enhanced by 1

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mg-C L-1 HA or FA, and the increases of bioaccumulation factors resulted from HA and FA were

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66% and 24% respectively, which indicated the high molecular weight DOM (HA) exert stronger

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influence on the bioaccumulation of perfluorooctanoic acid than the low molecular weight DOM

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(FA). In addition, the lower molecular weight DOM could pass through the biomembrane of

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organisms more easily compared to the higher molecular weight DOM,38 and thus the HOCs

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associated with lower molecular weight DOM might be taken up by organisms directly.

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Accordingly, it is very reasonable to hypothesize that the bioavailability of DOM-associated

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HOCs will vary with DOM molecular weight.

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Therefore, the aim of this research was to quantify the bioavailability of HOCs associated

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with DOM of various molecular weights. Pyrene and Daphnia magna were chosen as model HOC

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and organism respectively in this work. The improved passive dosing devices39,40 were made to

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maintain the freely dissolved pyrene concentration (Cfree) stable in the systems containing DOM

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with various molecular weights including >10K Da, 5-10K Da, 3-5K Da, 1-3K Da, and 10K Da), F2

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(5-10K Da), F3 (3-5K Da), F4 (1-3K Da), and F5 (10K Da) solutions after exposure for 144 h which was only 36 h later compared to that in

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AFW. However, after exposure for 144 h, the immobilization of Daphnia magna was only 30%

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and 0-40% in 10 mg-C L-1 middle molecular weight DOM (MMW DOM, 5-10K Da) and lower

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molecular weight DOM (LMW DOM, HMW, with

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the bioavailable fractions being 41.8%, 27.7%-32.5%, and 16.1%, respectively after exposure for

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48 h when the DOM concentration was 30 mg-C L-1.

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In addition, based on the relationship between the immobilization of Daphnia magna and the 15

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freely dissolved pyrene concentration (Cfree, µg L−1) in the absence of DOM (Figure S9), we

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could deduce the effective concentration of pyrene (Ceffective(2), µg L−1)40 causing the observed

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immobilization of Daphnia magna in systems containing DOM. As mentioned above, the food

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effect of 10 mg-C L-1 DOM was the same as 30 mg-C L-1 DOM. Therefore, the higher

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immobilization of Daphnia magna in the systems containing 30 mg-C L-1 DOM was caused by

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the difference between the pyrene associated with 30 mg-C L-1 DOM and 10 mg-C L-1 DOM.

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Consequently, the bioavailable fraction of DOM-associated pyrene (FDOM(2), %) based on the

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immobilization of Daphnia magna could be quantified with the following equation:

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‫ܨ‬ୈ୓୑(ଶ) =

஼౛౜౜౛ౙ౪౟౬౛యబ(మ) ି஼౛౜౜౛ౙ౪౟౬౛భబ(మ) [ୈ୓୑]యబ ×஼ీో౉యబ ି[ୈ୓୑]భబ ×஼ీో౉భబ

× 100%

(2)

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where Ceffective30(2) and Ceffective10(2) (µg L-1) were the effective concentrations of pyrene based on

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the immobilization of Daphnia magna in the systems containing 30 mg-C L-1 and 10 mg-C L-1

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DOM, respectively; [DOM]30 and [DOM]10 were 30 mg-C L-1 and 10 mg-C L-1 DOM in the

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systems, respectively; CDOM30 and CDOM10 (µg mg-1) were the concentrations of pyrene associated

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with DOM in the systems of 30 mg-C L-1 and 10 mg-C L-1 DOM, respectively. The obtained

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results are summarized in Table 1; the order of the bioavailable fraction of pyrene associated with

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DOM of various molecular weights was MMW > LMW > HMW. The bioavailable fractions of

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pyrene associated with MMW, LMW, and HMW DOM were 60.6%, 40.7%-48.9%, and 25.2%,

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respectively after exposure for 48 h when the DOM concentration was 30 mg-C L-1. They were

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higher than the results based on the pyrene content in tissues of Daphnia magna, and this

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suggested that DOM-mediated diffusive mass transfer effect and the indirect uptake of

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DOM-associated pyrene have promoted the accessibility of pyrene to Daphnia magna, enhancing

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the immobilization of Daphnia magna.

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3.5. Influencing Mechanisms of DOM Molecular Weight on the Bioavailability of

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DOM-Associated Pyrene to Daphnia magna

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3.5.1. Partition of Pyrene between DOM and Water 16

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The concentration of DOM-associated pyrene was highest in the HMW DOM solution,

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followed by MMW and LMW DOM solutions when the DOM concentration was identical in the

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systems; correspondingly, the Kdoc of pyrene between DOM and water was ordered as HMW >

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MMW > LMW (Table S5). For example, when the freely dissolved pyrene and DOM

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concentrations were 60 µg L-1 and 10 mg-C L-1 respectively, the LMW DOM-associated pyrene

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concentration was 3.04 × 106 - 3.57 × 106 µg kg-1, and the MMW and HMW DOM-associated

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pyrene concentrations were 5.90 × 106 and 1.10 × 107 µg kg-1 respectively; the Kdoc of pyrene in

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the systems with LMW DOM were 5.06 × 104 - 5.94 × 104 L kg-1, and that with MMW and HMW

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DOM were 9.84 × 104 and 1.84 × 105 L kg-1 respectively. In this research, the lg Kdoc of pyrene

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between DOM of various molecular weights and water ranged from 4.69 to 5.28, which were in

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the range (3.24-5.69) of the lg Kdoc values of pyrene between DOC of various types and water

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reported by Li et al.51

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3.5.2. Routes of DOM-Associated Pyrene Taken up by Daphnia magna

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The pollutants associated with DOM might be taken up by organisms through three routes:

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(1) transmembrane transport occurring on skin and gut wall; (2) endocytosis occurring on skin

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and gut wall; (3) desorbing from DOM or releasing from DOM degraded by digestive enzymes in

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the gut and taken up by organisms.52-54 Only pollutants associated with DOM of low molecular

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weight could be directly taken up by organisms through route (1). It is reported that LMW, however, the

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bioavailable fraction of pyrene associated with DOM was ordered as MMW > LMW > HMW.

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Since the bioavailable amount of pyrene was equal to the total amount of DOM-associated pyrene

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in the exposure solutions multiplied by the bioavailable fraction of pyrene associated with DOM,

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the net effect of Kdoc and bioavailable fraction led to that the pyrene content in the tissues of

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Daphnia magna excluding gut was the highest in the system of MMW DOM, followed by LMW

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DOM and HMW DOM when the freely dissolved concentration was identical as mentioned in

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section 3.3. It also resulted in that the additional immobilization caused by MMW DOM was

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higher than HMW DOM compared to the control group with only freely dissolved pyrene.

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3.6. Environmental Implications

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Many researchers suggest that the freely dissolved HOCs concentration is an indicator of

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bioavailability of HOCs. However, this study suggests that the DOM-associated pyrene was

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partly bioavailable to waterflea Daphnia magna, and the bioavailability of DOM-associated 19

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pyrene was influenced by the molecular weight of DOM. When freely dissolved pyrene

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concentration was 60 µg L-1, the pyrene content in the tissues of Daphnia magna in the systems

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containing 30 mg-C L-1 DOM with various molecular weights increased 42.1-92.2% compared to

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that in the control group without DOM. The results indicated that DOM-associated pyrene played

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an important role in the toxicity of pyrene in the exposure systems. Since DOM is ubiquitous in

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natural waters, it may not be suitable to consider the freely dissolved HOCs as the only

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bioavailable form; the bioavailability of DOM-associated HOCs should be taken into

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consideration in aquatic environments. Furthermore, the DOM concentration and structure will

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vary among the natural waters,56,57 and other water conditions including cations and pH values

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could influence the binding of HOCs to DOM.58,59 In addition, DOM effect on the bioavailability

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of HOCs also depends on the exposure regime.60 Consequently, the concentration, molecular

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weight, composition, and structure of DOM as well as other water conditions and the exposure

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regime should be considered when studying the bioavailability of HOCs in aquatic environments.

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The aquatic organisms are usually used to assess the bioavailability and toxic risks of HOCs

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in water systems. The utilization of DOM by organisms will depend on organism species with

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specific body length, body structures, and dietary habits, which will further influence the entry

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routes

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DOM-associated HOCs. Consequently, the organism species should be considered for the risk

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and bioavailability assessment of HOCs in water systems besides the DOM properties and water

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conditions, and more research should be conducted in this regard in the future. Especially, the

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direct uptake of DOM-associated HOCs by aquatic organisms needs further study.

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Supporting Information

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The Supporting Information is available free of charge on the ACS Publications website at DOI:

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of

DOM-associated

HOCs into organisms, thus affecting bioavailability of

Tables S1-S5 and Figures S1-S11 20

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Acknowledgements

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This work was supported by the National Key R&D program of China (2017YFA0605001),

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the National Natural Science Foundation of China (91547207), the National Science Foundation

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for Distinguished Young Scholars (51325902), and the National Natural Science Foundation for

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Innovative Research Group (51421065).

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References

484

(1) Smith, K. E. C.; Thullner, M.; Wick, L. Y.; Harms, H. Dissolved organic carbon enhances the

485

mass transfer of hydrophobic organic compounds from nonaqueous phase liquids (NAPLs) into

486

the aqueous phase. Environ. Sci. Technol. 2011, 45, (20), 8741-8747.

487

(2) Akkanen, J.; Vogt, R. D.; Kukkonen, J. V. K. Essential characteristics of natural dissolved

488

organic matter affecting the sorption of hydrophobic organic contaminants. Aquat. Sci. 2004, 66,

489

(2), 171-177.

490

(3) Schulten, H. R. Interactions of dissolved organic matter with xenobiotic compounds:

491

Molecular modeling in water. Environ. Toxicol. Chem. 1999, 18, (8), 1643-1655.

492

(4) Zheng, Z.; He, P. J.; Shao, L. M.; Lee, D. J. Phthalic acid esters in dissolved fractions of

493

landfill leachates. Water res. 2007, 41, (20), 4696-4702.

494

(5) Tolls, J. Sorption of veterinary pharmaceuticals in soils: A review. Environ. Sci. Technol.

495

2001, 35, (17), 3397-3406.

496

(6) Akkanen, J.; Tuikka, A.; Kukkonen, J. V. K. Comparative sorption and desorption of

497

benzo[a]pyrene and 3,4,3’,4’-tetrachlorobiphenyl in natural lake water containing dissolved

498

organic matter. Environ. Sci. Techno. 2005, 39, (19), 7529-7534.

499

(7) Marschner, B. Sorption of polycyclic aromatic hydrocarbons (PAH) and polychlorinated

500

biphenyls (PCB) in soil. J. Plant Nutr. Soil Sc. 1999, 162, (1), 1-14.

501

(8) Eriksson, J.; Frankki, S.; Shchukarev, A.; Skyllberg, U. Binding of 2,4,6-trinitrotoluene, 21

ACS Paragon Plus Environment

Environmental Science & Technology

502

aniline, and nitrobenzene to dissolved and particulate soil organic matter. Environ. Sci. Technol.

503

2004, 38, (11), 3074-3080.

504

(9) Lou, T.; Xie, H. X.; Chen, G. H.; Gagné, J. P. Effects of photodegradation of dissolved

505

organic matter on the binding of benzo(a)pyrene. Chemosphere 2006, 64, (7), 1204-1211.

506

(10) Tang, J. F.; Li, X. H.; Luo, Y.; Li, G.; Khan, S. Spectroscopic characterization of dissolved

507

organic matter derived from different biochars and their polycylic aromatic hydrocarbons (PAHs)

508

binding affinity. Chemosphere 2016, 152, 399-406.

509

(11) Chen, W.; Liu, X. Y.; Yu, H. Q. Temperature-dependent conformational variation of

510

chromophoric dissolved organic matter and its consequent interaction with phenanthrene. Environ.

511

Pollut. 2017, 222, 23-31.

512

(12) Akkanen, J.; Kukkonen, J. V. K. Measuring the bioavailability of two hydrophobic organic

513

compounds in the presence of dissolved organic matter. Environ. Toxicol. Chem. 2003, 22, (3),

514

518-524.

515

(13) Liu, Y. Z.; Yang, C.H.; Cheng, P.; He, X. J.; Zhu, Y. X.; Zhang, Y. Influences of humic acid

516

on the bioavailability of phenanthrene and alkyl phenanthrenes to early life stages of marine

517

medaka (Oryzias melastigma). Environ. Pollut. 2016, 210, 211-216.

518

(14) Moeckel, C.; Monteith, D. T.; Llewellyn, N. R.; Henrys, P. A.; Pereira, M. G. Relationship

519

between the concentrations of dissolved organic matter and polycyclic aromatic hydrocarbons in

520

a typical U.K. upland stream. Environ. Sci. Technol. 2014, 48, (1), 130-8.

521

(15) Xia, X. H.; Zhai, Y. W.; Dong, J. W. Contribution ratio of freely to total dissolved

522

concentrations of polycyclic aromatic hydrocarbons in natural river waters. Chemosphere 2013,

523

90, (6), 1785-1793.

524

(16) Xiao, Y. H.; Huang, Q. H.; Vähätalo, A. H.; Li, F. P.; Chen, L. Effects of dissolved organic

525

matter from a eutrophic lake on the freely dissolved concentrations of emerging organic

526

contaminants. Environ. Toxicol. Chem. 2014, 33, (8), 1739. 22

ACS Paragon Plus Environment

Page 22 of 34

Page 23 of 34

Environmental Science & Technology

527

(17) Qiao, P.; Farrell, A. P. Influence of dissolved humic acid on hydrophobic chemical uptake in

528

juvenile rainbow trout. Comp. Biochem. Phys. C. 2002, 133, (4), 575-585.

529

(18) Chen, S.; Ke, R. H.; Huang, S. B.; Sun, L. W.; Zha, J. M.; Wang, Z. J. Impact of dissolved

530

humic acid on the bioavailability of acenaphthene and chrysene assessed by membrane-based

531

passive samplers. Chinese Sci. Bull. 2007, 52, (19), 2642-2648.

532

(19) Akkanen, J.; Tuikka, A.; Kukkonen, J. V. K. On the borderline of dissolved and particulate

533

organic matter: Partitioning and bioavailability of polycyclic aromatic hydrocarbons. Ecotox.

534

Environ. Safe 2012, 78, 91-98.

535

(20) Perminova, I. V.; Grechishcheva, N. Y.; Kovalevskii, D. V.; Kudryavtsev, A. V.; Petrosyan, V.

536

S.; Matorin, D. N. Quantification and prediction of the detoxifying properties of humic

537

substances related to their chemical binding to polycyclic aromatic hydrocarbons. Environ. Sci.

538

Technol. 2001, 35, (19), 3841-3848.

539

(21) Yang, W. C.; Hunter, W.; Spurlock, F.; Gan, J. Bioavailability of permethrin and cyfluthrin in

540

surface waters with low levels of dissolved organic matter. J. Environ. Qual. 2007, 36, (6),

541

1678-85.

542

(22) Xia, X. H.; Rabearisoa, A. H.; Jiang, X. M.; Dai, Z. N. Bioaccumulation of perfluoroalkyl

543

substances by Daphnia magna in water with different types and concentrations of protein.

544

Environ. Sci. Technol. 2013, 47, (19), 10955-10963.

545

(23) Mayer, P.; Karlson, U.; Christersen, P. S.; Johnsen, A. R.; Trapp, S. Quantifying the effect of

546

medium composition on the diffusive mass transfer of hydrophobic organic chemicals through

547

unstirred boundary layers. Environ. Sci. Technol. 2005, 39, 6123-6129.

548

(24) Mayer, P.; Fernqvist, M. M.; Christersen, P. S.; Karlson, U.; Trapp, S. Enhanced diffusion of

549

polycyclic aromatic hydrocarbons in artificial and natural aqueous solutions. Environ. Sci.

550

Technol. 2007, 41, 6148-6155.

551

(25) Ter Laak, T. L.; Ter Bekke, M. A.; Hermens, J. L. M. Dissolved organic matter enhances 23

ACS Paragon Plus Environment

Environmental Science & Technology

552

transport of PAHs to aquatic organisms. Environ. Sci. Technol. 2009, 43, (19), 7212-7217.

553

(26) Smith, K. E. C.; Thullner, M.; Wick, L. Y.; Harms, H. Sorption to humic acids enhances

554

polycyclic aromatic hydrocarbon biodegradation. Environ. Sci. Technol. 2009, 43, (19),

555

7205-7211.

556

(27) Yang, Y.; Hunter, W.; Tao, S.; Gan, J. Microbial availability of different forms of

557

phenanthrene in soils. Environ. Sci. Technol. 2009, 43, (6), 1852-1857.

558

(28) Lam, B.; Baer, A.; Alaee, M.; Lefebvre, B.; Moser, A.; Williams, A.; Simpson, A. J. Major

559

structural components in freshwater dissolved organic matter. Environ. Sci. Technol. 2007, 41,

560

(24), 8240-8247.

561

(29) Zhao, Z. Y.; Gu, J. D.; Fan, X. J.; Li, H. B. Molecular size distribution of dissolved organic

562

matter in water of the pearl river and trihalomethane formation characteristics with chlorine and

563

chlorine dioxide treatments. J. Hazard. Mater. 2006, 134, (1-3), 60-66.

564

(30) Yoshioka, T.; Mostofa, K. M. G.; Konohira, E.; Tanoue, E.; Hayakawa, K.; Takahashi, M.;

565

Ueda, S.; Katsuyama, M.; Khodzher, T.; Bashenkhaeva, N.; Korovyakova, I.; Sorokovikova, L.;

566

Gorbunova, L. Distribution and characteristics of molecular size fractions of freshwater-dissolved

567

organic matter in watershed environments: its implication to degradation. Limnology 2007, 8, 29–

568

44.

569

(31) Wu, F. C.; Evans, D.; Dillon, P.; Schiff, S. Molecular size distribution characteristics of the

570

metal-DOM complexes in stream waters by high-performance size-exclusion chromatography

571

(HPSEC) and high-resolution inductively coupled plasma mass spectrometry (ICP-MS). J. Anal.

572

At. Spectrom. 2004, 19, (8), 979-983.

573

(32) Lin, H.; Chen, M.; Zeng, J.; Li, Q.; Jia, R. M.; Sun, X. W.; Zheng, M. F.; Qiu, Y. S. Size

574

characteristics of chromophoric dissolved organic matter in the Chukchi Sea. J. Geophys. Res.

575

Oceans 2016, 121, (8), 6403-6417.

576

(33) Kögel-Knabner, I.; Totsche, K. U.; Raber, B. Desorption of polycyclic aromatic 24

ACS Paragon Plus Environment

Page 24 of 34

Page 25 of 34

Environmental Science & Technology

577

hydrocarbons from soil in the presence of dissolved organic matter: effect of solution

578

composition and aging. J. Environ. Qual. 2000, 29, 906-916.

579

(34) Yu, H.; Huang, G. H.; An, C. J.; Wei, J. Combined effects of DOM extracted from site

580

soil/compost and biosurfactant on the sorption and desorption of PAHs in a soil-water system. J.

581

Hazard. Mater. 2011, 190, (1-3), 883-890.

582

(35) Gourlay, C.; Tusseau-Vuillemin, M. H.; Garric J.; Mouchel, J. M. Effect of dissolved organic

583

matter of various origins and biodegradabilities on the bioaccumulation of polycyclic aromatic

584

hydrocarbons in Daphnia. Environ. Toxicol. Chem. 2003, 22, (6), 1288-1294.

585

(36) Chin, Y. P.; Aiken, G. R.; Danielsen, K. M. Binding of pyrene to aquatic and commercial

586

humic substances: The role of molecular weight and aromaticity. Environ. Sci. Technol. 1997, 31,

587

(6), 1630-1635.

588

(37) Xia, X. H.; Dai, Z. N.; Rabearisoa, A. H.; Zhao, P. J.; Jiang, X. M. Comparing humic

589

substance and protein compound effects on the bioaccumulation of perfluoroalkyl substances by

590

daphnia magna in water. Chemosphere 2015, 119, 978-986.

591

(38) Rosenstock, B.; Zwisler, W.; Simon, M. Bacterial consumption of humic and non-humic low

592

and high molecular weight DOM and the effect of solar irradiation on the turnover of labile DOM

593

in the southern ocean. Microb. Ecol. 2005, 50, (1), 90-101.

594

(39) Smith, K. E. C.; Dom, N.; Blust, R.; Mayer, P. Controlling and maintaining exposure of

595

hydrophobic organic compounds in aquatic toxicity tests by passive dosing. Aquat. Toxicol. 2010,

596

98, (1), 15-24.

597

(40) Zhang, X. T.; Xia, X. H.; Li, H. S.; Zhu, B. T.; Dong, J. W. Bioavailability of pyrene

598

associated with suspended sediment of different grain sizes to daphnia magna as investigated by

599

passive dosing devices. Environ. Sci. Technol. 2015, 49, (16), 10127-10135.

600

(41) Gouliarmou, V.; Smith, K. E. C.; de Jonge, L. W.; Mayer, P. Measuring binding and

601

speciation of hydrophobic organic chemicals at controlled freely dissolved concentrations and 25

ACS Paragon Plus Environment

Environmental Science & Technology

602

without phase separation. Anal. Chem. 2012, 84, (3), 1601-1608.

603

(42) Xia, X. H.; Li, H. S.; Yang, Z. F.; Zhang, X. T.; Wang, H. T. How does predation affect the

604

bioaccumulation of hydrophobic organic compounds in aquatic organisms? Environ. Sci. Technol.

605

2015, 49, (8), 4911-4920.

606

(43) Dong, J. W.; Xia, X. H.; Wang, M. H.; Lai, Y. J.; Zhao, P. J.; Dong, H. Y.; Zhao, Y. L.; Wen, J.

607

J. Effect of water-sediment regulation of the xiaolangdi reservoir on the concentrations,

608

bioavailability, and fluxes of PAHs in the middle and lower reaches of the Yellow River. J.

609

Hydrol. 2015, 527, 101-112.

610

(44) OECE Guidelines for the testing of chemicals; organization for economic co-operation and

611

development: paris, 2008.

612

(45) Mcmeans, B. C.; Koussoroplis, A. M.; Arts, M. T.; Kainz, M. J. Terrestrial dissolved organic

613

matter supports growth and reproduction of daphnia magna when algae are limiting. J. Plankton

614

Res. 2015, 37, (6), 1201-1209.

615

(46) Kwon, J. H.; Escher, B. I. A modified parallel artificial membrane permeability assay for

616

evaluating the bioconcentration of highly hydrophobic chemicals in fish. Environ. Sci. Technol.

617

2008, 42, (5), 1787-1793.

618

(47) Reichenberg, F.; Mayer, P. Two complementary sides of bioavailability: accessibility and

619

chemical activity of organic contaminants in sediments and soils. Environ. Toxicol. Chem. 2006,

620

25, (5), 1239-1245.

621

(48) Cui, X. Y.; Mayer, P.; Gan, J. Methods to assess bioavailability of hydrophobic organic

622

contaminants: Principles, operations, and limitations. Environ. Pollut. 2013, 172, 223-234.

623

(49) Roditi, H. A.; Fisher, N. S.; Sanudo-Wilhelmy, S. A. Uptake of dissolved organic carbon and

624

trace elements by zebra mussels. Nature, 2000, 407, (6800), 78-80.

625

(50) Voets, J.; Bervoets, L.; Blust, R. Cadmium bioavailability and accumulation in the presence

626

of humic acid to the zebra mussel, Dreissena polymorpha. Environ. Sci. Technol. 2004, 38, (4),

627

1003-1008.

628

(51) Li, Y. L.; He, W.; Liu, W. X.; Kong, X. Z.; Yang, B.; Yang, C.; Xu, F. L. Influences of 26

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Page 26 of 34

Page 27 of 34

Environmental Science & Technology

629

binding to dissolved organic matter on hydrophobic organic compounds in a multi-contaminant

630

system: Coefficients, mechanisms and ecological risks. Environ. Pollut. 2015, 206, 461-468.

631

(52) Nardi, S.; Pizzeghello, D.; Muscolo, A.; Vianello, A. Physiological effects of humic

632

substances on higher plants. Soil Biol. Biochem. 2002, 34, (11), 1527-1536.

633

(53) Tan, L. Y.; Huang, B.; Xu, S.; Wei, Z. B.; Yang, L. Y.; Miao, A. J. TiO2 nanoparticle uptake

634

by the water flea daphnia magna via different routes is calcium-dependent. Environ. Sci. Technol.

635

2016, 50, (14), 7799-7807.

636

(54) Gophen, M.; Geller, W. Filter mesh size and food particle uptake by Daphnia. Oecologia

637

1984, 64, (3), 408-412.

638

(55) Vicentini, M.; Morais, G. S.; Rebechi-baffio, D.; Richardi, V. S.; Santos, G. S.; Cestari, M.

639

M.; Navarro-Silva, M. A. Benzo(a)pyrene exposure causes genotoxic and biochemical changes in

640

the midge larvae of chironomus sancticaroli strixino & strixino (diptera: chironomidae). Neotrop.

641

Entomol. 2017, 46, 658-665.

642

(56) Kikuchi, T.; Fujii, M.; Terao, K. M.; Jiwei, R.; Lee, Y. P.; Yoshimura, C. Correlations

643

between aromaticity of dissolved organic matter and trace metal concentrations in natural and

644

effluent waters: a case study in the Sagami River Basin, Japan. Sci. Total Environ. 2017, 576,

645

36-45.

646

(57) Stolpe, B.; Zhou, Z. Z.; Guo, L. D.; Shiller, A. M. Colloidal size distribution of humic- and

647

protein-like fluorescent organic matter in the northern Gulf of Mexico. Mar. Chem. 2014, 164,

648

25-37.

649

(58) Xia, X. H.; Rabearisoa, A. H.; Dai, Z. N.; Jiang, X. M.; Zhao, P. J.; Wang, H. T. Inhibition

650

effect of Na+ and Ca2+ on the bioaccumulation of perfluoroalkyl substances by Daphnia magna in

651

the presence of protein. Environ. Toxicol. Chem. 2015, 34, (2), 429-436.

652

(59) Mei, Y.; Bai, Y. C.; Wang, L. Y. Effect of pH on binding of pyrene to hydrophobic fractions

653

of dissolved organic matter (DOM) isolated from lake water. Acta Geochim. 2016, 35, (3), 27

ACS Paragon Plus Environment

Environmental Science & Technology

654

288-293.

655

(60) Tejeda-Agredano, M. C.; Mayer, P.; Ortega-Calvo, J. J. The effect of humic acids on

656

biodegradation of polycyclic aromatic hydrocarbons depends on the exposure regime. Environ.

657

Pollut. 2014, 184, 435-442.

658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 28

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Table 1. Bioavailable fraction of DOM-associated pyrene to Daphnia magna

680

(Average of three replicates, RSD < 10%) Based on the pyrene content in the tissues of Daphnia magna

DOM molecular weight and concentration

Cfree of pyrene (µg L-1)

Bioavailable fraction of DOM-associated pyrene (%) 48 h

Based on the immobilization of Daphnia magna Cfree of pyrene (µg L-1)

Bioavailable fraction of DOM-associated pyrene (%) 36 h

48 h

10 K Da (30 mg-C L-1)

60.0

16.1

20.0

25.7

25.2

681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 29

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Immobilization (%)

100

20 µg L-1 pyrene Control 10K Da

80 60 40 20 0 0

Immobilization (%)

100

12

24

36

48

24

36

48

24

36

48

40 µg L-1 pyrene Control 10K Da

80 60 40 20 0 0

Immobilization (%)

100

12 60 µg L-1 pyrene Control 10K Da

80 60 40 20 0 0

707

12

Time (h)

708

Figure 1. Effects of DOM (10 mg-C L-1) with different molecular weights on the immobilization

709

of Daphnia magna at different freely dissolved pyrene levels during a 48-h exposure (mean ±

710

standard deviation, n = 3). Control means without DOM, and the immobilization of Daphnia

711

magna was zero in the solutions of DOM without pyrene during a 48-h exposure.

712

713

714

715

716 30

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100

-1

Immobilization (%)

20 µg L pyrene Control

80

-1

10 mg-C L DOM (5-10K Da) -1

30 mg-C L DOM (5-10K Da)

60 40 20 0 0 100

12

24

36

48

-1

Immobilization (%)

20 µg L pyrene Control

80

-1

10 mg-C L DOM (>10K Da) -1

30 mg-C L DOM (>10K Da)

60 40 20 0 0

12

24

36

48

Time (h)

717 718

Figure 2. Effects of MMW and HMW DOM concentrations on the immobilization of Daphnia

719

magna during a 48-h exposure. (mean ± standard deviation, n = 3). Control means without DOM,

720

and the immobilization of Daphnia magna was zero in the solutions of DOM without pyrene

721

during a 48-h exposure.

722

31

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100

-1

Immobilization (%)

60 µg L pyrene