Seagrass beds acting as a trap of microplastics - Emerging hotspot in the coastal region?

Journal Pre-proof Seagrass beds acting as a trap of microplastics - Emerging hotspot in the coastal region? Yuzhou Huang, Xi Xiao, Caicai Xu, Yuvna Devi Perianen, Jing Hu, Marianne Holmer PII:

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DOI:

https://doi.org/10.1016/j.envpol.2019.113450

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ENPO 113450

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Environmental Pollution

Received Date: 31 March 2019 Revised Date:

27 September 2019

Accepted Date: 20 October 2019

Please cite this article as: Huang, Y., Xiao, X., Xu, C., Perianen, Y.D., Hu, J., Holmer, M., Seagrass beds acting as a trap of microplastics - Emerging hotspot in the coastal region?, Environmental Pollution (2019), doi: https://doi.org/10.1016/j.envpol.2019.113450. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.

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Seagrass beds acting as a trap of microplastics - emerging hotspot in the coastal region?

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Yuzhou Huang1, Xi Xiao1,2,3*, Caicai Xu1, Yuvna Devi Perianen1, Jing Hu1, Marianne Holmer1,3

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1

Ocean College, Zhejiang University, 1 Zheda Road, Zhoushan, Zhejiang 316021, China

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2

Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, MNR,

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HangZhou, 310012, China

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3

9

Denmark

Department of Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M,

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Corresponding author:

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Dr. Xi Xiao,

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[email protected], Telephone: +86-15088785518,

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Fax: +86-0580 2092891.

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Abstract: Microplastics is an emerging environmental problem in the world. However, presence

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and fate of microplastics in seagrass meadows are barely known. In this study, the abundance

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and diversity of microplastic from Enhalus acodoides vegetated sites and bare sites were

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quantified and characterized in Xincun bay and Li’an bay, Hainan, China. Microplastics ranged

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from 80.0‒884.5 particles per kg of dry sediment, and fibers were the dominant shape. The most

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frequent colors of microplastics were blue, transparent and black. The dominant size of

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microplastics was in the range of 125‒250 µm. And the seagrass sediments were enriched in

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microplastics 2.1 and 2.9 times for Xincun bay and Li’an bay, respectively. The trap effect of

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seagrass was non-selective regarding the shape, color and size of microplastics. High

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anthropogenic pollution and poor beach management may contribute to higher concentrations of

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microplastics in Li´an bay.

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Keywords: Microplastics; Seagrass; Trap effect; Enrichment

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1.

Introduction

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Microplastics have become a new environmental problem in the oceans in recent years. Plastic

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particles, with the size between 0.001 and 5 mm, are defined as microplastics (Koehler et al.,

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2015). They can be further divided into primary and secondary microplastics according to their

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origin (Koehler et al., 2015). Primary microplastics are produced as small particles, like drug

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delivery media and microbeads in cosmetics and toothpaste (Shim et al., 2018), whereas

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secondary microplastics are derived from the gradually breaking down of larger plastic pieces

38

under the effect of solar radiation, temperature, biological and physical damage (Weinstein et al.,

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2016). By 2100, the average concentration of microplastics in surface seawater is expected to

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reach 9.8‒48.8 particles m-3 and the average concentration on beaches will reach 1580‒8050

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particles kg-1 dry sediment, if no actions are taken to reduce the release of plastics to the

42

environment (Everaert et al., 2018). Furthermore, while microplastics themselves are

43

contaminants, they also adsorb chemical compounds to the surface due to high sorption capacity

44

(Hwang et al., 2014) and pass them through the biological food webs. Worldwide studies have

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shown that microplastics carry high levels of chemical contaminants in many places (Wang et al.,

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2018; Zhang et al., 2018) such as heavy metals found adhering to microplastics at Brazil beaches

47

(Brennecke et al., 2016; Vedolin et al., 2017) and polycyclic aromatic hydrocarbons (PAHs)

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adsorbing to microplastics in Xiamen coastal areas, China (Tang et al., 2018).

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At present, wetland is not only playing important functions including biodiversity support,

51

nutrient cycling and floodwater buffering, but also acts as a hub of microplastic transmission in

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the global ecosystem (Liu et al., 2019; Zedler, 2000). As one of the important wetland and blue

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carbon ecosystems, seagrass meadows are significant global carbon sinks and contribute to

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global climate change mitigation (Gullstrom et al., 2018). It is well known that seagrasses can

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slow down the water flow velocity, enhance retention of particles and increase sedimentation

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(Bostrom et al., 2010; Butman et al., 1988; Gacia et al., 1999). The blue carbon stocks in

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seagrass meadow are not only provided by the carbon derived from seagrasses, but also by

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external carbon sources including phytoplankton, macroalgae, mangrove detritus and terrestrial

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sources (Rohr et al., 2016). The fact that seagrass meadows act as a trap of particulate matter

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suggests that, seagrass meadows may also serve as a significant trap of microplastics. In the

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marine environment microplastics are generated from coastal fishing activity, driven by winds

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and currents from the beaches (Veerasingam et al., 2016), transported by rivers, effluents from

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industrial plants and sewage to coastal zone, where for example sewage-discharges is an

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important source of fibers from washing clothes (Lebreton et al., 2017; Mark Anthony et al.,

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2011). Fibers are the most dominant microplastics found in subtidal areas (Shim et al., 2018).

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Microplastics have been found attached to the surface of Thalassia hemperichii leaves, which

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increase the possibility of uptake of microplastics by herbivores and thus enter into the food web

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(Goss et al., 2018). Interestingly, the probability of recovering microplastics in shellfish and fish

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in the Mediterranean is 46.3% and 47.2%, respectively, with an average of ~ 2 items/individual

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(Digka et al., 2018). In China, the microplastics contents in market bivalve is as high as 4.3‒57.2

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items/individual (Li et al., 2015). Seagrasses are not only a direct food source for many

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herbivores, such as dugongs and sea turtles (Short et al., 2011), but also a major nursery ground

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for near shore fauna (Dahlgren et al., 2006). Commercial fisheries are important in seagrass

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meadows all over the world (Nordlund et al., 2018), and if microplastics accumulate in seagrass

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beds, there is a risk of exposing the food web in the seagrasses to microplastics and their

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contaminants, which may affect the natural species and eventually fisheries. Therefore, it’s of

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primary importance to investigate the possible trap effect of microplastics by seagrasses.

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Due to the impact of human activities, seagrass meadows are now suffering myriad of threats,

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i.e., damaging fisheries practices, coastal construction, eutrophication and sediment loading, and

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the global seagrass meadow area is rapidly decreasing (Short et al., 2011). Xincun (XC) bay and

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Li’an (LA) bay in Hainan Province are hot-spots for seagrass research in China (Huang et al.,

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2006). The seagrass meadow in XC and LA bay are under high anthropogenic pressures, and

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large patches of coral reefs had disappeared in two bays (Fang et al., 2018). The area percentage

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of extremely human activity in XC bay was 6.67%, while 13.53% in LA bay (Fang et al., 2018),

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although a marine reserve for seagrass was established in the XC bay in 2007 (Yang and Yang,

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2009).

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Therefore, in this study, we investigated the concentration and diversity of microplastics in the

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sediments of the seagrass meadows in XC bay and LA bay, and compared them with adjacent

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non-vegetated area. Our hypotheses were 1) the abundance and diversity of microplastic are

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higher inside the seagrass meadow compared to bare sites; and 2) the abundance and diversity of

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microplastic are higher in LA bay compared to XC bay due to higher pressure of human

95

activities.

96 97

2.

Material & method

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2.1 Field works and pretreatment of samples

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XC bay and LA bay, hosting two important fishing ports, are located in the southeast of Hainan

100

island (18°24′‒18°27′ N, 109°58′‒110°4′ E), and are similar in geology, with only one narrow

101

channel connected to the South China Sea (Fig. 1). The main force driving water flow in two

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lagoons is the irregular diurnal tide. Tourism and marine aquaculture are developed in XC Bay,

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and the bay has more than 3.2 km2 aquaculture area and an area of 22.5 km2 with an average

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water depth of 4.2 m, and a tidal range of 0.7 m. LA bay has more than 2.4 km2 aquaculture area

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and an area of 7.9 km2, at water depth of 5.5 m and a tidal range of 0.6 m (Fang et al., 2018; Gu

106

et al., 2016; Zhou et al., 2017). Seagrasses covered 2.0 km2 and 3.2 km2 of sand-mud beaches in

107

XC and LA bay in 2002, respectively (Huang et al., 2006), but the meadows have been declining

108

due to high anthropogenic pressures since that time (Yang and Yang, 2009). Significant amounts

109

of plastic waste were observed along the beaches in both bays.

110 111

Sediments and seagrass were sampled from monospecific meadows of Enhalus acodoides and

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non-vegetated sites in the intertidal zone of XC bay and LA bay, in January 2018. Non-vegetated

113

sites were randomly selected in the same area as the seagrass sites to ensure similar exposure to

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microplastics in the vegetated and non-vegetated sites. Non-vegetated sites were located outside

115

the seagrass beds ~ 10 m away from its boundary. Around 10 intact seagrass shoots were

116

randomly dug out in the vegetated site. Then, the seagrass shoots were washed thoroughly and

117

the youngest 2 leaves of every shoot were sampled to measure organic carbon and nitrogen

118

content and 13δC and 15δN. Epiphyte samples were scraped lightly from the shoots by use of a

119

razor blade. Microphytobenthos (MPB) were carefully collected by syringe by sampling the

120

upper 2 mm of the surface sediments. For each site, ~ 2 kg surface sediment (0‒5 cm depth) was

121

collected using stainless-steel shovel, which was sufficient to make 3 subsamples of a total of

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450 g dry sediment per site. In the laboratory each of the replicate wet sediment sample was

123

homogenized in an aluminum tray and air dried at room temperature.

124

125 126

Fig. 1. Sampling sites in Xincun bay and Li’an bay located in the southeast Hainan Island.

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2.2 Microplastics extraction

129

Microplastics were extracted by standard density separation approach using the Munich Plastic

130

Sediment Separator (MPSS, HYDRO-BIOS Ltd, Kiel, Germany) from the dried sediments.

131

Recovery rate quantification experiment showed that the MPSS method has high recovery rate

132

of small microplastic particles (S-MPP, < 1 mm) and large microplastic particles (L-MPP, 1‒5

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mm), which are up to 90.8 ± 8.7% and 100 ± 0%, respectively (Table S2, Fig. S2). The overall

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recovery rate was 94.8 ± 7.9% with a detection limit of 8 µm. Saturated Zn solution (1.69

135

g/cm3) was used as separation solution and stored in a 20 L glass tank. Purified water (Milli-Q

136

Advantage A10, Millipore Corporation, MA, USA) was used for rinsing. The operation steps of

137

MPSS was modified from the Schmid’s method (Imhof et al., 2012). Briefly, 150 g of dry weight

138

samples was ultrasound-assisted dissolute in Zn solution for 5 min. Then the sediment

139

solution was poured into a rotating sediment container, and mixed in saturated Zn solution

140

for 15 min with a rotational speed of 4‒8 rpm (Lorenz, 2014) and then left to settle. After 90 min,

141

~ 100 ml solution was transferred to a beaker (500 ml) and the dividing chamber was rinsed with

142

purified water for three times into the same beaker.

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Finally, 8 ml HCl (38‒40%) and 30 ml 30% H2O2 were added in the solution to dissolve shells

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and digest organic matter. After reaction for 48 hour, the solution was left in pear type separating

146

funnels for 24 hour. Then each solution was filtered using nitrocellulose membrane (pore size: 8

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µm; Xinya Ltd., Jinjing, China), and the membrane was stored in a Petri dish for air drying at

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room temperature. Blank control (without sediment samples added) was set up following the

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same procedure.

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2.3 Microplastics identification

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The particles on the nitrocellulose membrane were identified using stereomicroscope (SOPTOP

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SZN, Sunny Instruments Co., Ltd, Ningbo, China). Non-microplastic particles were filtered out,

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if not confirmed by a further spectral analysis using Fourier Transform Infrared spectrometer

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(FTIR, Nicolet iS50, ThermoFisher). The FTIR was fitted with an ATR accessory (ATR-FTIR),

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which has a ZnSe crystal on a single reflection crystal plate and a pressure clamp. The spectra is

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a mid-IR range of 650 and 4000 cm-1. Wave resolution was set at 4 cm-1 and the rate was 32

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scans per analysis (Mohamed Nor and Obbard, 2014). All spectra were compared with the

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spectra in Hummel Polymer Sample Library and HR Nicolet Sampler Library from Nicolet iS50

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software. At least three representative particles of each types were selected from every filter (155

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particles in total) and were scanned by FTIR (Duncan et al., 2018; Mohamed Nor and Obbard,

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2014; Zhou et al., 2018).

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The length and width of each microplastics were measured by microscope with assistant of the

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Algae Counting software (Wseen Detection Technology Co., Ltd. Hangzhou, China). The

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microplastic abundances were calculated as particles kg-1 dry sediment weight (particles kg-1

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DW). According to Nor and Obbard (2014), microplastics were classified by shape (fiber,

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fragment, pellet, film and foam) (Free et al., 2014), color (black, white, blue, red, transparent,

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green and others) and size (lengths: 8‒20 µm, 20‒31 µm, 31‒63 µm, 63‒125 µm, 125‒250 µm,

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250‒500 µm, 500‒1000 µm and 1000‒5000 µm) (Kedzierski et al., 2016; Rocha-Santos and

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Duarte, 2015).

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2.4 Enrichment index and diversity index of microplastics

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Enrichment index was calculated by the equation:

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EI = (1)





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where Av is the microplastic abundance in the vegetated area; and Ab is the microplastic

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abundance in the bare sites. EI > 1 represents that microplastics were enriched in the vegetated

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area.

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Diversity index was calculated by the equation (Jost, 2010; Wang et al., 2019):

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D (MP) = 1 − ∑      =  ! " (2)

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S is number of microplastic categories; N is total number of microplastic in a sample; q is

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relative abundance of microplastic categorized into the ith type; ni is the number of microplastic

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categorized into the ith type.

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The microplastic shape-color diversity index (shape-color D’(MP)) was calculated based on the

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combination of shape (5 types) and color (7 types) information. And the size-based diversity

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index (size D’(MP)) based on size categories was also calculated.

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2.5 Plant and sediment characteristics

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Different seagrass tissues, epiphytes removed from seagrass leaves by razor blade and MPB

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were dried in oven at 60°C for 48 hour. The density of sediment was determined by pre-weighed

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plastic syringe with known volume. Wet weight of sediment subsamples was dried for 12 hour at

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105°C to calculate water content (β). Porosity (φ) was calculated from water content and density.

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Dried sediments were analyzed for stable isotopes of carbon and nitrogen (13C and 15N),

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Particulate Organic Carbon (POC), and Particulate Organic Nitrogen (PON) content. All samples

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were analyzed with Thermo Scientific, delta V advantage, isotope ratio mass spectrometer (with

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Vienna Peedee belemnite as reference material) connected to elemental analyzer. Plants were

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dried for 48 hour at 60°C and analyzed for isotopic composition and POC and PON content.

198 199

2.6 Statistical analysis

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Data analysis were performed using Matlab R2017b (Mathworks Corporation, Massachusetts,

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USA) and Origin Pro 9.0 (Origin Lab Corporation, Massachusetts, USA). Geographic map of

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sampling sites in Hainan was drawn by Arc GIS10.5 (ESRI, California, USA). Levene statistic

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and Shapiro-Wilk statistic were used to test the homogeneity and normality of variance. Analysis

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of variance (ANOVA) was conducted using SPSS 20.0 (IBM SPSS Statistics, Chicago, USA)

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following Tukey post hoc test. When p < 0.05, the value was considered statistically significant.

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3.

Results

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3.1 Abundance of microplastics in/outside E. acoroides meadow

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The polymer types of microplastics consisted of polyethylene (PE), polypropylene (PP),

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polyamide 6 (PA), and polystyrene (PS), according to the spectra scanned by ATR-FTIR (Fig.

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2&3). 39 out of 155 particles were identified as microplastics. The most abundant polymer types

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were PE (48.7%) and PP (33.3%), following with PA (10.3%) and PS (7.7%). In XC bay, the

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concentration of microplastics in the bare and vegetated sites were 93.3 ± 15.3 and 196.7 ± 16.1

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particles kg-1 DW, respectively. In LA bay, the concentration of microplastic was 267.1 ± 60.5

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particles kg-1 DW in the bare site; and up to 780.2 ± 147.0 particles kg-1 DW in the vegetated site

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(Fig. 4). The blank controls contained 5.0 ± 1.7 particles, showing good quality of contamination

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control during the lab procedures. For both bays, the microplastic abundance at vegetated sites

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were significantly higher than the corresponding bare sites (p < 0.01). The enrichment index of

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microplastic in the seagrass sites compared to bare sites was 2.1 and 2.9, respectively in XC and

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LA bay. In addition, the microplastic concentration in LA bay was significantly higher than XC

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bay (p < 0.01; Fig. 4).

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Fig. 2. Typical microplastics in the sediment of Xincun bay and Li’an bay. a: red fiber with color fading; b: transparent

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thick fiber; c: blue fragment; d: black film; e: black pellet; f: white foam.

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Fig. 3. FT-IR spectra of microplastics isolated from the sediment samples and the standard spectra of plastics. a:

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polyethylene, b: polypropylene, c: polyamide 6, and d: polystyrene. Up: spectra of microplastics isolated from the

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sediment samples; down: the standard spectra from spectra library.

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Fig. 4. Microplastics abundance of sediments in the bare and vegetated sites of Xincun bay and Li’an bay. Lower case

231

letter indicated statistics significance among the four sampling sites (Tukey test, p < 0.05).

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3.2 Diversity of microplastics in/outside vegetated meadow: shape, color and size

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1) Shape. Fiber was the most abundant shape category at almost all sites (on average 58.6% ±

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16.0%), with XC vegetated showing the highest contribution (71.5%). The only exception was

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the vegetated site in LA, where fragment was the most abundant (43.1% ± 4.8%, Fig. 5). The

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next abundant shape was fragment, accounting for 27.7% ± 12.0% of all the microplastics. Film

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was the third most abundant, accounting for 11.5% ± 6.5% on average. Foam was only found at

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the vegetated site in LA. Fiber percentage in XC bay was significantly higher than LA bay (p <

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0.01), while fragment in XC bay was significantly lower than LA bay (p < 0.05). And there was

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no significant difference of all shape between vegetated and non-vegetated sites. Microplastics

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contamination during experiment found in the blank control only consisted of fibers.

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2) Color. The most abundant color of microplastics was blue (40.0% ± 11.3%) followed by

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transparent (18.2% ± 8.9%) and black (13.2% ± 5.9%) (Fig. 5). The blue microplastics in the

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bare site of XC bay was highest (54.2% ± 5.9%), and was significantly higher than the bare site

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in LA bay (p < 0.01). Transparent and green were significantly different among four sampling

249

sites (p < 0.05). However, black, red and white microplastics didn’t show significant difference

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among four sampling sites (p > 0.05).

251 252

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Fig. 2. Shape (left) and color (right) of microplastic in the bare and vegetated sites of Xincun bay and Li’an bay. ‘X’

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means no particle of this shape found in the site. Lower case letters indicated significant differences among the four

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sampling sites for each shape independently (Tukey test, p < 0.05).

257 258

3)

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± 8.9%), following by 63‒125 (20.6% ± 9.5%) and 31‒63 µm (17.3% ± 7.0%). Microplastics

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with size range of 1000‒5000 µm was the lowest (Fig. 6). In the range of 125‒250 µm, LA bare

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site had the highest percentage of 36.9% ± 4.0%, following by XC vegetated and XC bare, 26.3%

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± 2.5% and 22.7% ± 9.7%, respectively. Only size 20‒31 µm group exhibited significant

263

difference among four sampling sites according to ANOVA, which was higher in LA vegetated

Size. According to the length, microplastics concentrated in the range of 125‒250 µm (26.3%

264

than XC bare.

265

4) Diversity index. In the bare sites, shape-color D’(MP) was significantly higher in the LA bay,

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comparing to the XC bay (p < 0.05). However, no significant different was found inside and

267

outside the seagrass vegetation for these two bays. Shape-color D’(MP) in LA bay was

268

significantly higher than XC bay (p < 0.01). The size D’(MP) showed no significant difference

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between two bays and in/outside vegetation (Table 1).

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Table 1. Microplastic shape-color diversity and size-based diversity indexes of sediments in the bare and vegetated sites

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of Xincun bay and Li’an bay (mean ± S.D.). Lower case letter indicated significant differences among the four sampling

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sites (Tukey test, p < 0.05). Sample sites

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Shape-color D’(MP)

Size D’(MP)

XC bare

0.78±0.02

b

0.77±0.04a

XC vegetated

0.80±0.04ab

0.79±0.01a

LA bare

0.84±0.01a

0.77±0.03a

LA vegetated

0.85±0.01a

0.82±0.01a

275 276

Fig. 6. Size classification of microplastics in the bare and vegetated sites of Xincun bay and Li’an bay.

277 278

3.3 Sediment characteristics

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The density of sediment was significantly higher in LA bay with 1.83 ± 0.03 g/cm3, as compared

280

to XC bay (1.73 ± 0.03 g/cm3). Average content of POC in LA bay was 0.23 ± 0.08% which was

281

0.07% higher as compared to XC bay (0.16 ± 0.03%). Content of PON in LA vegetated site was

282

the highest (0.03 ± 0.00%) among all the sampling sites. The δ13C of sediment was same for

283

both LA bay (-13.64 ± 1.19%) and XC bay (-13.46 ± 0.32%). The δ15N of sediment was also

284

same for both LA bay (5.02 ± 0.59%) and XC bay (5.54 ± 0.57%) (Table 2).

285 286

The POC of the Enhalus acodoides leaves was 3.96% higher for the LA bay compared to the XC

287

bay. Also, the PON of the Enhalus acodoides leaves was 0.85% higher in LA bay as compared to

288

XC bay. Besides, the PON of the Enhalus acodoides roots was found to be 1.06% higher in LA

289

bay in comparison to XC bay; where PON may reflect higher nutrient contents in their growing

290

environment (Table 3). Similar phenomenon was found for the epiphytes and MPB in the two

291

bays; the POC for epiphytes was 12.94% higher in LA bay in comparison to XC bay.

292

the POC for MPB was 8.05% higher in LA bay compared to XC bay. In addition, the PON for

293

epiphytes was 1.38% higher in LA bay compared to XC bay, the PON for MPB was 0.89%

294

higher in LA bay in comparison to XC bay. The δ15N in all the seagrass tissues (leaf, root and

295

rhizome), epiphytes and MPB were higher by 1.63%, 5.40%, 3.68%, 3.95% and 0.83%,

296

respectively in LA bay as compared to XC bay.

Moreover,

297 298

Table 2. Sediment characteristics, carbon and nitrogen content and isotopic values in the bare and vegetated sites of

299

Xincun bay and Li’an bay (mean ± S.D., n=2-4). Lower case letter indicated significant differences among the four

300

sampling sites (Tukey test, p < 0.05).

301 Sample sites Density(g/cm3)

303 304 305

Porosity

POC (%)

PON (%)

C/N

δ13C (%)

δ 15N (%)

XC bare

1.71±0.03b

19.95±0.27c 0.34±0.01c

0.14±0.01

0.01±0.00

19.84±1.23

-13.73±0.16

5.65±0.33

XC vegetated

1.76±0.02b

21.87±0.40b 0.38±0.01b

0.18*

0.02±0.00

11.65*

-13.19±0.04

5.44±0.91

LA bare

1.82±0.02a

22.42±0.16a 0.41±0.00a

0.16±0.02

0.01±0.00

15.18±0.71

-14.60±0.74

4.56±0.41

0.30±0.01

0.03±0.00

12.55±0.43

-12.68±0.08

5.48±0.18

LA vegetated

302

(%)

1.84±0.03

a

20.40±0.13

* only one replicate for this sample.

c

0.38±0.01

b

306 307

Table 3. Carbon, nitrogen and isotopic values of Enhalus acodoides tissues (leaf, roots, and rhizomes), epiphytes and

308

microphytobenthos (MPB) in Xincun bay and Li’an bay.

Li’an bay

Xincun bay

POC (%) PON (%)

C/N

δ 13C (%) δ 15N (%)

Ea leaves

31.86

3.64

10.20

-8.46

5.65

Ea roots

34.11

0.68

58.27

-9.18

4.16

Ea rhizomes

28.20

2.64

12.48

-7.62

6.07

Epiphytes

11.02

1.58

8.13

-12.08

8.18

MPB

1.67

0.12

16.69

-7.78

7.30

Ea leaves

35.82

4.49

9.31

-6.65

7.28

Ea roots

32.13

1.74

21.55

-7.05

9.56

Ea rhizomes

22.08

1.85

13.95

-6.81

9.75

Epiphytes

23.96

2.96

9.43

-12.95

12.13

MPB

9.72

1.01

11.19

-7.03

8.13

309 310 311

4

Discussion

312

4.1 Seagrass beds acting as a trap of microplastics

313

Our result showed that the microplastic abundance in vegetated sites were significantly higher

314

than those of the bare sites, with an enrichment factor of 2.1 and 2.9 in XC bay and LA bay,

315

respectively. To our knowledge, this is the first documentation of a trap effect of microplastics

316

by seagrass beds, which is consistent with high particle retention in seagrass meadows (Gacia et

317

al., 1999). We also observed significantly higher organic carbon in the vegetated sediment of two

318

bays (Table 2), which proved that particulate organic matter was enriched in the sediment due to

319

the presence of seagrasses. In the seagrass beds, the bottom roughness and the benthic boundary

320

layer are larger compared to bare site, which increase the friction and reduces the water flow

321

(Linders et al., 2018). The water flow is reduced from to 2 to >10 times by the canopy, the

322

resuspension of sediment is less and the sediment accumulation rate and accumulation of organic

323

particles are higher (Abdelrhman, 2003; Duarte et al., 2013; Fonseca et al., 2019; Gacia et al.,

324

1999; Miyajima et al., 2015; Rohr et al., 2018; Wahyudi et al., 2016). Seagrass canopy can affect

325

particle flux directly through loss of momentum when particles are caught by leaves and sink

326

into the seagrass bed (Hendriks et al., 2008; Linders et al., 2018). Similarly, microplastics may

327

be trapped in the seagrass beds due to the lower water flow and increased particle collisions with

328

leaves. Furthermore, microplastics and other particles may stick to seagrass leaves or to

329

epiphytes (Goss et al., 2018), and accumulate in the sediments when the leaves are buried.

330

Similar to our findings, sheltered intertidal mudflats with low physical disturbance showed

331

higher microplastic abundance than exposed sand beaches (Lo et al., 2018). The fact that the

332

blue carbon ecosystems are accumulating marine plastic litter would also help explain its trap

333

effect of microplastics. For instance, in the Red Sea and the Arabian Gulf, mangroves were

334

observed to be the sinks of marine plastic litter by trapping them from marine and terrestrial

335

debris (Martin et al., 2019). Interestingly, the accumulation of plastics in the mangroves was

336

twice as high as the bare sites, which is similar to the enrichment effect of the vegetation found

337

in this study for the microplastics. Hence, seagrasses (E. acodoides) appear to trap microplastics

338

from the water column and seagrass meadows can be considered as reservoirs of microplastic in

339

the marine environment. This accumulation of microplastics may increase the exposure of

340

seagrass flora and fauna to anthropogenic contaminants. Microplastics may also have negative

341

effects on seagrass by altering sediment structure and bulk density (Rillig et al., 2019).

342

Meanwhile, contaminants adsorbed to microplastics may affect seagrass root traits and growth in

343

a similar way like terrestrial plants (de Souza Machado et al., 2019; Rillig et al., 2019). In fact,

344

seagrass leaves with microplastics attached have been identified as potential vector for

345

microplastics entering the food web (Goss et al., 2018). Microplastics may cause physical

346

blockage in organisms and accumulation of non-nutrient elements in their stomachs leading to

347

starvation (Boerger et al., 2010; Zhou et al., 2018). In addition, microplastics themselves may

348

leach adhered pollutants from environment, like PCBs, PAHs and DDTs (Wang et al., 2018),

349

exposing benthic organisms in seagrass sediments to pollutants. Since seagrass beds are

350

important fishery areas in the global scale (Nordlund et al., 2018), microplastics accumulated in

351

the seagrass beds may impose potential threat to human beings through food web (Barboza et al.,

352

2018). On the other hand, seagrass beds have a high sediment bury rate (Marba et al., 2015) and

353

act as a trap of microplastics. Therefore, it could also reduce the microplastics left in the aquatic

354

environment.

355 356

4.2 Size, shape and color of microplastics

357

Most of the microplastics found in this study were smaller than 1 mm (> 98 %), which can be

358

easily ingested by marine biota (Zhou et al., 2018). Size is a key factor to the bioavailability,

359

biological effect, microplastics migration and contamination adsorption of microplastics (Shim

360

et al., 2018; Wright et al., 2013). Smaller size microplastics have lower settling velocity and

361

migrate longer from the source (Kedzierski et al., 2016; Khatmullina and Isachenko, 2017).

362

When water flow is reduced in seagrass bed smaller size microplastics may be filtered out and

363

settle in the sediments. Smaller size microplastics have higher threat to environment due to high

364

surface volume ratio for pollutants adsorption and biota availability (Wang et al., 2018; Zhou et

365

al., 2018). However, our results showed that the percentage of small size microplastics in this

366

shallow water environment is similar inside and outside the seagrass beds probably due to

367

significant mixing of the sediments during tides and storms.

368 369

The dominant shape of microplastics was fiber, which is abundant in subtidal zones too (Shim et

370

al., 2018). Washing of clothes (Mark Anthony et al., 2011), fishing net and fishing rope (Yong et

371

al., 2014) are important sources of fiber microplastics. Fibers are commonly ingested by marine

372

turtles, bivalves and macro fauna living in seagrass beds (Duncan et al., 2018; Li et al., 2015;

373

Remy et al., 2015). Fiber (i.e. fishing lines etc.) has a lower settling velocity than other shapes of

374

microplastic (Khatmullina and Isachenko, 2017), and a higher fraction of fibers in seagrass

375

meadows compared to outside could thus be expected. However, our survey reveals that the

376

percentage of fiber microplastics in and outside of seagrass beds are the same probably due to

377

tides and storms as discussed above. By now, settling velocity of microplastic size has only been

378

tested for sizes ranging from ~ 500 to 5000 µm (Khatmullina and Isachenko, 2017; Kooi et al.,

379

2016), which where only a small portion of the microplastics found in our study and further

380

studies of settling velocity of small size (< 500 µm) microplastic are needed to understand the

381

settling pattern of fibers in seagrass sediments.

382 383

Blue is the most common color of microplastics, followed by transparent, found in sediments

384

and water column in general around the world, and even plankton ingestion is predominately

385

blue (Duncan et al., 2018; Gago et al., 2018). In this study, blue was found to be the dominating

386

color of microplastics, and then following by transparent and black, similar to mangrove

387

sediments in Singapore and similar to findings in marine turtles in the Atlantic ocean, in the

388

Mediterranean and in the Pacific ocean (Duncan et al., 2018; Mohamed Nor and Obbard, 2014).

389

The color of microplastics plays a role in relation to adsorption of chemical contaminants, which

390

is higher in black microplastics (Wang et al., 2018). Further, fibers dyed by industrial dyes,

391

especially Direct Red 28, is causing carcinogenicity in vertebrates (Remy et al., 2015). The color

392

of microplastics also plays a role of bioavailability due to food resemblance. Biotas tend to prey

393

white, tanned or opaque microplastics mistakenly comparing to other colors (Shaw and Day,

394

1994; Wright et al., 2013). The abundance of marine biota is higher in seagrass beds, and marine

395

biotas forage in seagrass beds at the same time. Consequently, the percentage of white

396

microplastics in the sediment was supposed less than the bare sites, while percentage of

397

transparent microplastics was higher than the bare sites hypothetically. Our results showed that

398

the accumulation of black and white microplastics was the same in vegetated and bare sites,

399

while only transparent group complied with this hypothesis in the XC bay. Further studies are

400

needed to explore the role of colors in seagrass sediments.

401 402

4.3 Comparison between the two bays

403

Higher concentration of microplastics was found in LA bay as compared to XC bay (Fig. 4).

404

This may be partially due to higher anthropogenic pollution in LA bay (Mohamed Nor and

405

Obbard, 2014; Zhou et al., 2018), as reflected by the higher nutrient levels in the sediment of LA

406

bay; higher nutrient levels and 15N values in the seagrass tissues and epiphytes of LA bay. In fact,

407

13.5% of the area in LA is defined to have extreme human activity, while this is only 6.7% in

408

XC bay (Fang et al., 2018). Furthermore, beach management may also contribute to the

409

difference of microplastic abundance between these two bays, similar as the research of

410

microplastic distribution in the coasts of the Bohai Sea and the Yellow Sea (Zhou et al., 2018).

411

Beaches in XC bay were cleaned regularly, whereas garbage was piling up on the beaches in LA

412

bay. Significantly higher concentration of fibers (and lower fragment concentration) was found

413

in XC bay, as compared to the LA bay, which may be due to sewage with higher percentage of

414

fibers as an important source of microplastic in XC bay (Mark Anthony et al., 2011).

415 416

5.

Conclusion

417

Seagrass (Enhalus acodoides) meadows showed significant trap effect of microplastics and the

418

trap effect was amplified in microplastic-rich region emphasizing the filtering capacity of

419

seagrasses. The seagrass meadows showed non-selective enrichment to microplastics regarding

420

their color, size and shape. Higher microplastic levels were found in the more eutrophic location,

421

which were exposed to more severe anthropogenic pollution. Further observations in a larger

422

geographical range and of sub-tidal meadows, are urgently required to understand the trapping

423

effect of microplastic by blue carbon ecosystem. A complete environmental assessment of the

424

risk of microplastics to flora and fauna in seagrass ecosystem is urgently needed given the high

425

trapping efficiency of microplastics.

426 427

Acknowledgements

428

We thank Prof. Haibo Zhang at the Zhejiang A&F University, Prof. Huahong Shi and his

429

scientific team at the East China Normal University, and Prof. Yungui Ma and Assoc. Prof.

430

Xuegang Chen at Zhejiang University for valuable guides on the methodology. Prof. Marianne

431

Holmer thanks to the short-term 1000 talent project from Zhejiang Province. This study was

432

supported by the National Natural Science Foundation of China (21677122 & 21876148), the

433

National Key R and D Program of China (2016YFC1402104), the Major Science and

434

Technology Program for Water Pollution Control and Treatment (2018ZX07208-009), the open

435

fund of the Key Laboratory of Integrated Marine Monitoring and Applied Technologies for

436

Harmful Algal Blooms, SOA (MATHAB201809), the open fund of the Laboratory of Marine

437

Ecosystem, Biogeochemistry, Second Institute of Oceanography, SOA (LMEB201709), China

438

Scholarship Council (201806325035) and the Fundamental Research Funds for the Central

439

Universities.

440 441

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Microplastics were trapped in the sediment by seagrasses in the vegetated sites with an enrichment factor 2.1 and 2.9 in Xincun bay and Li’an bay respectively. Microplastics abundance ranged from 80.0 - 884.5 particles per kg of dry sediment in Xincun and Li’an bay. Fiber among shapes, blue among color and small microplastics size ranged (125 250 µm) were the most abundant types. High anthropogenic pollution and poor beach management may contribute to higher concentrations of microplastics.

The authors have no conflicts of interest to declare.