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Science of the Total Environment 762 (2021) 144110

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Modelling the accumulation of microplastics through food webs with the


example Baiyangdian Lake, China
Yi-fei Ma, Xue-yi You ⁎
Tianjin Engineering Center of Urban River Eco-purification Technology, School of Environmental Science and Engineering, Tianjin University, Jinnan District, Tianjin 300350, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Accumulation of MPs in aquatic organ-


isms was different with trophic levels.
• MPs abundance in aquatic organism and
environment related to rainfall intensity
• MPs abundance in aquatic organisms
and environment with respect to time
was found.
• More delay of MPs accumulation be-
tween trophic levels for higher
trophic level

a r t i c l e i n f o a b s t r a c t

Article history: Microplastic plastics (MPs) is an increasingly widely serious global environment problem, which severely threats
Received 24 October 2020 aquatic organisms and even human beings. However, the potential change trend of MPs abundance over time in
Received in revised form 20 November 2020 natural aquatic ecosystems and the cumulative effects through food webs are unclear. In this research, the model
Accepted 21 November 2020
of accumulation effect of MPs through aquatic food webs was established in the example Baiyangdian Lake
Available online 15 December 2020
(China) using the contaminant tracer module Ecotracer in the Ecopath modelling software. The results indicated
Editor: Damia Barcelo that the MPs spread and accumulate throughout the food-web fast, and finally to the high trophic level aquatic
organisms, Snakehead. The abundance of MPs in aquatic environment and organisms varies periodically with
Keywords: rainfall. The abundance of MPs in snakehead, mandarin fish, common carp, crucian carp, chub, fingerling, grass
Microplastics carp, mollusc, microzoobenthos, zooplankton increased about 3.97, 2.87, 2.35, 1.8, 1.48, 1.8, 1.86, 1.98, 1.99, 3.49
Baiyangdian Lake times of the initial abundance of MPs in them, respectively. Since snakehead exists in the highest trophic level
Ecotracer in Baiyangdian Lake ecosystem, the cumulative effect of MPs is the most serious through food web. Furthermore,
Food-web the accumulation of MPs in different trophic levels has a time delay effect, and the higher the nutrient level is, the
Aquatic organisms
more obvious the delay effect is. The results also showed that Ecotracer is a good model to explore the enrich-
ment effect of MPs in food web, the accumulation of MPs through food webs is serious, and the phenomenon
should arouse serious attention.
© 2020 Elsevier B.V. All rights reserved.

1. Introduction mechanical constraints (Cole et al., 2011). MPs have attracted world-
wide attention due to its universality and persistence in aquatic envi-
Microplastics (MPs) are plastic particles with particle size smaller ronments (Andrady, 2011). Studies have shown that MPs can be easily
than 5 mm (Kershaw and Rochman, 2016), it mainly come from ingested by aquatic organisms due to they are similar in size to the lar-
manufactured for industrial or domestic use, or as a result of large vae of several organisms, including plankton (Besseling et al., 2014).
items gradually broken down under biological, chemical and/or However, the effect of MPs on aquatic organisms are diverse (Wright
et al., 2013), not only limited to ingestion, but also transferred to tissues
⁎ Corresponding author. (Von et al., 2012; Fleurine et al., 2020; Tu et al., 2018). Von et al. (2012)
E-mail address: xyyou@tju.edu.cn (X. You). firstly found that the transfer of MPs from the digestive tract to tissue in

https://doi.org/10.1016/j.scitotenv.2020.144110
0048-9697/© 2020 Elsevier B.V. All rights reserved.
Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

invertebrate (M. edulis) under laboratory conditions. Tu et al. (2018) et al., 2020), therefore, rainfall was considered to calculate the base in-
found that the MPs can be ingested by zooplankton and further affect flow rate of MPs in aquatic environment.
its growth and reproduction. Fleurine et al. (2020) found the MPs in The aims of this study are: (1) Study the influence of rainfall on the
non-edible (gills, digestive system) and edible (muscle) flesh of some variation of base inflow rate on MPs abundance in aquatic environment;
seafood samples under natural conditions, which demonstrate that (2) Detect the variation of MPs abundance inwater in natural environ-
MPs can enter the tissues of aquatic organisms by ingestion or respira- ment; (3) Simulate the variation of MPs abundance in aquatic organ-
tion and stay for a long time. The MPs entering the organism will di- isms; (4) Find the mechanism of MPs transfer and accumulation
rectly damage and block the digestive tract, resulting in the decrease among different trophic levels; (5) Assess the enrichment degree of
of feeding efficiency, energy shortage, growth retardation and other MPs through food web; (6) Provide suggestions for people's dietary
problems. It will also aggravate the toxicity to organisms through the choices and MPs control.
adsorption of heavy metals and persistent organic pollutants (POPs),
and even lead to the death of individual organisms (Derraik, 2002; 2. Area of study
Jabeen et al., 2017).
Furthermore, Rochman et al. (2015) evaluated the fish and shellfish Our study area is Baiyangdian lake (38°43′–39°02′N, 115°38′–116°–
sold for human consumption in the world and found that more than half 07′E), which is located in the center of Hebei province with an area of
of aquatic products contain human plastic products, which indicates 366 km2 (Fig. 1). It is 39.5 km from east to west and 28.5 km from
that MPs may eventually enter the human body through diet. The inter- north to south. The average annual precipitation is 550 mm and the av-
action between MPs and human body will produce allergy, cytotoxicity, erage annual evaporation is 1637 mm. Precipitation varies greatly from
immune response or other acute reactions, and ultimately endanger year to year, and about 89.7% rainfalls are from May to October.
human health (Campanale et al., 2020). However, the research on trans- Baiyangdian Wetland is the biggest natural freshwater wetland and
fer and accumulation mechanism of MPs through food-web under nat- important aquatic products base in North China Plain. It plays an impor-
ural environments is scarce. tant role in maintaining local ecological balance. Due to the influence of
In order to detect the transfer and accumulation mechanism of MPs natural conditions and human activities, the runoff of rivers has de-
in aquatic organisms through food-web, the combination of ecotoxicol- creased and a large number of waste water from urban domestic sew-
ogy and food-web modelling is important to address the impacts of pol- age, industrial and agricultural has been discharged in recent years.
lutants at the ecosystem level. Ecotracer is an effective model to Since there are many plastic products used in life, agricultural produc-
modelling the spread and accumulation of pollutants or toxins (Booth tion and industrial manufacturing, it has caused a serious plastic pollu-
and Zeller, 2005; Booth et al., 2020). However, it has not been applied tion in water.
to the study of MPs spread and accumulation in aquatic system at pres-
ent. In this approach, the model of accumulation effect of MPs through 3. Methods
aquatic food webs was established in the example Baiyangdian Lake
(China) using the contaminant tracer module Ecotracer. From previous 3.1. Ecopath model
studies, we know that runoff may be one of the important ways in
which terrestrial plastic particles are transferred to water (Su et al., Ecopath is a modelling software of ecosystem that the assumption of
2018) and rainfall is the most effective way to form surface runoff (Xia steady-state parameters to generate an energy flow network is applied

Fig. 1. Location of Baiyangdian Wetland.

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

by the standing stocks and trophic interactions of functional groups in mortality rate (i.e., non-predation mortality), Ei is the emigrating bio-
an ecosystem over a period of time. The balance of mass (energy, nutri- mass rate (/year), mi (/year) is the excretion and/or metabolic rate,
ents) for any functional group (i) was obtained by setting its production and di (/year) is the physical decay rate.
to be equal to the sum of consumption components and expressed as: The abundance of MPs in the environment is also related to inflow
      and loss. Inflow originates from the release of pollutants into the envi-
P n Q P
¼∑ Bj DC ij þ Ei þ Y i þ B ð1−EEi Þ ð1Þ ronment as inflow rate, and from the excretion from organisms. Losses
B i j¼1 B j B i i originate from physical decay rates, base volume exchange and the di-
rect uptake by organisms from the environment.
where, the left side of the equation is expressed as the rate between the The environmental compartment can be expressed as:
production (Pi) and biomass (Bi). The terms of right-hand side are the
sum of the predation terms expressed as the product of the consump- dC 0 ðt Þ
¼ α i −βi C 0 ðt Þ ð5Þ
tion of biomass ratio (Q/Bj), the predator biomass (Bj) and the propor- dt
tion of the prey i in the diet of predator j (DCij). The net flow through
the boundaries of system is dispersal (Ei). The fishing exploitation is where, αi represents the gains in environment and βi represents the
represented by the catches (Yi). The accumulation or depletion of bio- losses to environment.
mass is BAi. The non-predation natural mortality is expressed by means
n
of ectotrophic efficiency (EEi). α i ¼ BI þ ∑ mi Ai ð6Þ
The basic parameters to establish Ecopath model are Bi (P/B)i (Q/B)i, i

EEi and DCji and only three above parameters are needed and the left
one can be calculated by the model. Normally, EEi is hard to get directly, where, BI is the inflow rate (items/km2/year) to environment, and miAi
therefore we used the model to calculate it. When the resulting system are the excretory products from all organisms within the environment.
of equations was solved, it provided a snapshot of the flows within a tro- n
phic web (Christensen and Pauly, 1993; http://www.ecopath.org). In βi C 0 ¼ ðdi þ V i ÞC 0 þ ∑ μ i Bi C 0 ð7Þ
i
order to fulfill the condition of steady state, the model was balanced
by ensuring the values of EEi < 1 and 0.1 < P/Q < 0.35 of fish species
where, di represents the decay rate (/year), and Vi represents the base
(Tuda and Wolff, 2018). If the model didn't satisfy mass balance, the
volume exchange loss (/year). Temporal changes through environmen-
input parameter should be adjusted properly until the model reached
tal concentration C0 can be made by applying a forcing function to in-
a steady state (Christensen et al., 2004).
flow rate or through a contaminant concentration driver file.
3.2. Ecotracer model
3.3. Determination of model data
Ecotracer as a pollutant module of Ecopath, uses the biomass flow
The food web of Baiyangdian lake was described through the
between functional groups and the environment to predict the concen-
Ecopath with Ecosim food web model which consists 13 biological
tration of pollutants that are passively flowing with biomass of food
groups and one detritus group. The food web model was shown basi-
web. It is assumed that pollutants follow biomass passively and instan-
cally to represent the whole Baiyangdian ecosystem (Yang and Chen,
taneously. The MPs amount of a group depends on intake and loss. Up-
2013). The biomass of 14 functional groups, P/B and Q/B value in the ini-
take comes from the direct uptake rate (i.e., respiration), losses arise
tial year 2009 were acquired from the reference of Yang et al. (2011).
from natural decay processes, metabolic losses and emigration.
The amount of fishing and fishing mortality which driving Ecosim mod-
Ecotracer is based on a standard dynamic transfer model:
ule was obtained through the economic statistical yearbook of Baoding
dC i ðt Þ City. The diet composition in Ecopath (Table 1) was concluded from the
¼ α i −βi C i ðt Þ ð2Þ
dt previous published papers (Cao and Shi, 1996; Cao et al., 2003; Han and
Li, 1995; Li, 1994; Liu et al., 2011; Li et al., 2014) and the data released in
where, αi represents the gains from direct uptake from environment the web (http://www.fishbase.org/).
plus the gains from diet, and βi represents the losses due to physical de- In considering the MPs abundance in the lakes, the MPs concentra-
cay and elimination rates, which are dependent upon the group's tions of water was found to be mainly determined by the variable of an-
concentrationCi. nual rainfall, local GDP and industrial output of fiber and plastics and
these variables value can be found in Economic Statistical Yearbook.
Aj
α i ¼ μ i Bi C 0 þ AEi ∑ Q ji þ ci I i ð3Þ Using these data, the relation of the MPs concentrations and annual
j¼prey Bj
rainfall, local GDP and industrial output of fiber and plastics was
found. The data were shown in Table 2.
where, Co represents the environmental concentration (items/km2), Bi
The relation of the MPs abundance in the lakes and the surrounding
is the biomass (t) of group i, μiis the direct absorption rate proportional-
human actives was determined by the measured data in Tai Lake, Chao
ity co-efficient linking the direct uptake rate (items/km2/year) to the
Lake, Dianshan Lake (Jiang et al., 2018; Su et al., 2018; Xiong et al., 2018;
parameters of biomass (t/km2) and environmental concentration
Fraser et al., 2020). The relation was also verified by the measured data
(items/km2), AEi is the assimilation efficiency and it is the fraction of
of Poyang Lake, South Dongting Lake, Gaoyou Lake and it was found that
MPs within food items that is assimilated, Qji is the consumption rate
the relation can predict the MPs abundance in the lakes well. Therefore,
(items/year) of group j by group i,Ajis the amount (MPs) of the contam-
the initial MPs concentration of Baiyangdian Lake in 2009 was esti-
inant present in group j andBjis the biomass of prey group j(t), ci is the
mated by the following relation (Ma and You, 2020a).
group biomass concentration (items/t), and Ii is the immigrating bio-
mass (t/year). M ¼ 0:00823 x þ 0:52508 y þ 0:095 z ð8Þ
 
Q ij
βi ¼ ∑ þ F i þ MOi þ Ei þ mi þ di ð4Þ where, x is GDP; y is annual precipitation; z is industrial output of fiber
j¼pred Bi
and plastics; M is the abundance of MPs in water.
Using Eq. (8), the initial abundance of MPs in Baiyangdian Lake in
where, Qij is the rate of consumption (items/year) of group i due to pre- 2009 was estimated to be 306.14 items/L, which was changed into the
dation by j, Fi is the fishing mortality rate (/year),MOi(/year) is the other unit required by Ecotracer as 0.110412 × 1010 items/km2.

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

Table 1
Diet composition matrix for the functional groups in Ecopath module of Baiyangdian Lake.

Predator prey 1 2 3 4 5 6 7 8 9 10

Snakehead
Mandarin fish 0.021
Common carp 0.119
Crucian carp 0.753
Chub 0.0538
Grass carp
Fingerling 0.0535
Mollucs 0.02 0.05 0.01
Microzoobenthos 0.3 0.0025 0.163
Zooplankton 0.317 0.253 0.141 0.0015 0.05 0.02 0.05
Submerged plant 0.371 0.68 0.239 0.986 0.996
Emergent plant 0.131
Phytoplankton 0.312 0.325 0.666 0.014 0.2 0.25
Detritus 0.183 0.787 0.78 0.7

Note: The number from 1 to 10 corresponds to the functional group in the left column from up to bottom.

Table 2
Statistics of annual precipitation, GDP and the industrial output of fiber and plastics and the measured MPs in the lakes.

Variable\lake Tai Lake Poyang Lake South Dongting Lake Chao Lake Gaoyou Lake Dianshan Lake

GDP (billion Chinese Yuan) 30,626 13,631 5169 7946 1604 27.8
Annual precipitation (mm) 1219 1874 1364 1661 941 1566
Industrial output of fiber and plastics (million Chinese Yuan) 14,292 1512 404 658 2188 814
MPs (item/m3) 2250 1100 967 1000 1711 900

The inflow rate of MPs in 2009 of Baiyangdian Lake was estimated by 2018; Li et al. (2020a); Li et al. (2020b); Jiang et al., 2020). Decay rate
using the fitting formula between the increase of abundance of MPs and of organisms refers to the proportion of MPs in intestinal tract to total
rainfall. The formular fitted by the experimental data of Xia et al. (2020) MPs in organism and it was set according to Tu et al. (2018), Huang
was y = 3.379 ln(x) + 5.3516 and R2 = 0.703. Considering Baiyangdian et al. (2020), Koongolla et al. (2020). The proportion of contaminant ex-
Lake is surround by many large cities, the actual inflow rate of MPs of creted is the number of MPs that does not enter tissues after ingestion, it
Baiyangdian Lake is similar to that of Lake Donghu, we used the formula was set according to Fleurine et al. (2020), Li et al. (2020a, 2020b). The
fitted by the experimental data of Xia et al. (2020) to estimate the in- input parameters of Ecotracer were shown in Table 4. The model runs
crease of MPs in Baiyangdian lake and the inflow rate of MPs of forward in time with using Ecosim components to estimate potential
Baiyangdian Lake was 26.5457 items/L in 2009, which converts to the concentrations of functional groups and species for lacking such data
unit required by Ecotracer as 0.009574 × 1010 items/km2/year. Since under environmental steady-state conditions.
the inflow rate of MPs is related to rainfall, the monthly inflow of MPs
from 2009 to 2016 was set as a forcing function shown in Table 3. Be- 4. Results
cause surface runoff is not formed in Baiyangdian Lake in cold winter,
no basic inflow rate of MPs from November to February of the next 4.1. Ecopath model
year is considered. The rainfall data in 2009–2016 in Baiyangdian Lake
were obtained in Economic statistical yearbook. Food web is also called food chain web or food cycle. Ecopath model
For organisms, we assumed that the abundance of MPs in the same is a common method to study the function and structure of food web.
kind of fish of two lakes is the same if the two lakes have similar key When using the Ecopath model, it should be assured of balance of
food web and the abundance of MPs in water. Due to the lack of the each organism at first. The output parameters of Ecopath in 2009 were
measured data in Baiyangdian Lake, we cited the measured abundance listed in Table 5. It was found that the values of Ecotrophic efficiency
of MPs in similar freshwater such as Tai Lake and Poyang Lake as the ini- (EEi) < 1 and (Production/Consumption) P/Q are in the range of
tial MPs concentration in organisms (Jabeen et al., 2017; Jiang et al., 0.1–0.35 of fish groups which indicates that the model is in a balanced
2020; Sun et al., 2018; Li et al. (2020a); Li et al. (2020b); Zhou et al. state.
(2020)). The direct absorption rate was set according to the measured The structure and trophic levels (TLs) of key food web of
data in gills (Lars-Henrik et al., 2016) in above researches (Tu et al., Baiyangdian Lake ecosystem were shown in Fig. 2 and Table 6,

Table 3
Monthly inflow of MPs in Baiyangdian lake in 2009–2016. Unit:items/l.

Year 2009 2010 2011 2012 2013 2014 2015 2016

Month

3 18.3 18.66 0 13.1 8.31 9.06 6.72 0


4 20.98 20.05 16.64 18.77 15.23 17.88 18.17 14.43
5 19.48 18.89 18.08 14.32 17.17 18.96 22.39 18.75
6 22.02 17.15 22.38 22.53 23.99 21.87 17.65 23.76
7 24.68 22.28 26.48 25.74 25.04 20.5 24.1 27.03
8 25.35 24.81 23.14 23.6 22.55 22.21 24.57 24
9 22.19 23.33 20.03 22.36 21.09 21.89 21.81 20.67
10 15.21 15.45 14.83 13.86 14.29 14.53 15.17 15.89

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

Table 4
Input parameters of starting values of Ecotracer baseline simulation in Baiyangdian Lake.

Group Initial conc. Conc. in immigrating biomass Direct absorption rate Decay rate Prop. of containment excreted
(items/t × 1010) (items/t) (items/t/year) (items/year) [0–1]

Snake head 0.0008 0 0.1098 0.0346 0.675


Mandarin fish 0.00003 0 0.0366 0.0067 0.686
Common Carp 0.00003 0 0.0366 0.256 0.686
Crucian Carp 0.0001 0 0.0732 0.8 0.686
Chub 0.0021 0 0.0732 0.128 0.686
Grass Carp 0.0005 0 0.11 0.0128 0.686
Fingerling 0.0006 0 0.0542 0.128 0.686
Mollucs 0.0002 0 0.0289 0.0116 0.618
Microzoobenthos 0.0002 0 0.00449 0.0116 0.618
Zooplankton 0.00000008 0 0.00449 0.0116 1
Submergent Plant 0 0 0 0 1
Emergent Plant 0 0 0 0 1
Phytoplankton 0 0 0 0 1
Detritus 0.00006 0 0 0 1

Table 5
The output parameters of Ecopath in 2009.

Group Biomass in habitat area (t/km2) Production/biomass (/year) Consumption/Biomass (/year) Ecotrophic efficiency Production/consumption

Snake head 3.84 1.3 7 0.175 0.186


Mandarin fish 0.5 1.4 7.2 0.994 0.194
Common Carp 19.2 1.9 8.8 0.211 0.216
Crucian Carp 134.41 2.1 7.4 0.184 0.284
Chub 9.6 2.3 8.5 0.168 0.271
Grass Carp 9.6 2.5 9 0.094 0.278
Fingerling 7.68 2.15 8.1 0.198 0.265
Mollucs 22 3 12.876 0.913 0.233
Microzoobenthos 7 20 62.5 0.707 0.32
Zooplankton 3.9 113 389.655 0.824 0.290
Submergent Plant 2600 1.25 0.154
Emergent Plant 1200 1 0.109
Phytoplankton 37.11 85.891 0.264
Detritus 70 0.250

Fig. 2. Trophic relationships of functional groups of Baiyangdian Lake ecosystem in 2009 (The number under the name of the species represents the biomass of groups. The black curve
represents the predation relationship and the number in the left represent the trophic levels of groups).

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

Table 6 inflow rate, which brings MPs from land to water and MPs settled into
Nutrition level and food chain quantity of each functional groups in the sediment fast (Ma and You, 2020b).
Baiyangdian Lake.

Group name Number of paths Trophic level 4.2.2. The variation of MPs abundance in aquatic organisms
Snakehead 52 3.302 Fig. 4 showed the variation of MPs abundance with respect to time in
Mandarin fish 10 2.347 aquatic organisms. It showed that the abundance of MPs in aquatic or-
Common Carp 12 2.331 ganisms appeared periodicity variation, which similar to the abundance
Crucian Carp 12 2.327
of MPs in water environment. What's more, it showed that all abun-
Chub 11 2.161
Grass Carp 2 2 dance of MPs in aquatic organisms was increased at the end of simula-
Fingerling 7 2.004 tion. However, there were different degrees of increase. The
Mollucs 7 2.219 accumulation of MPs in aquatic organisms at the top of the trophic
Microzoobenthos 4 2.021 level or that on the bottom layer which mainly feeds detritus was the
Zooplankton 2 2.053
Total 119 2.286
highest.
Fig. 5 showed that the abundance of MPs in aquatic organisms before
and after the simulation (2009–2016). It was found that the abundance
respectively. Four trophic levels were considered in Baiyangdian Lake of MPs in snakehead, mandarin fish, common carp, crucian carp, chub, fin-
ecosystem. The TL of major economic fishes was 2.161–2.347 with an gerling, grass carp, mollusc, microzoobenthos, zooplankton increased
average of 2.286. The functional group at the top of TL was snakehead about 3.97, 2.87, 2.35, 1.8, 1.48, 1.8, 1.86, 1.98, 1.99, 3.49 times as
whose nutrition reached 3.302. Among the consumers, grass carp was much as the initial abundance of MPs in them, respectively. Since
at the bottom of TL. This is because grass carp directly feeds on sub- snakehead exists in the highest trophic level in Baiyangdian Lake ecosys-
merged plants and phytoplankton. tem, the cumulative effect of MPs is the most serious through food web.
From Fig. 2, it was seen that there were two kinds of energy flow in The accumulation effect in zooplankton was also high, it was due to zoo-
Baiyangdian Lake ecosystem. The first was the predatory food chain, and plankton feed on detritus and phytoplankton, which the MPs are rich.
the second was the detritus food chain. There were 119 food chains in MPs with large diameter settled down into sediment (detritus) fast
Baiyangdian Lake ecosystem. Among them, snakehead had the largest (Ma and You, 2020b). Most MPs with small particle size distributed
number of 52 food chains. The lowest number of food chain was the near water surface and attached to the surface of phytoplankton, which
groups of zooplankton and grass carp, both of which were 2 food chains leads to the accumulation of MPs in zooplankton due to predation.
because zooplankton feeds on detritus and phytoplankton and grass carp Fig. 6 showed the variation of MPs abundance in aquatic organisms
only feed on submerged plants and phytoplankton. in four seasons (take 2015 as an example). It was found that the MPs
in aquatic organisms in spring was the lowest since there was less rain-
fall in Baiyangdian area and the abundance of MPs flowing from land to
4.2. Ecotracer model water was low. In addition, most of the MPs accumulated in aquatic or-
ganisms in the summer and autumn of last year were reduced after the
4.2.1. The variation of MPs abundance winter. With the increase of rainfall in summer, the MPs abundance
The variation of MPs abundance with respect to time in water envi- flowing from land to Baiyangdian Lake was increased, which further
ronment was shown in Fig. 3. It was found that the MPs abundance in lead to the increase of MPs abundance in aquatic organisms. The MPs
water appeared periodicity variation with the rainfall in seasons and abundance in aquatic organisms in autumn was steady or slightly grow-
the MPs abundance in water reached the peak value in rainy season ing. On the one hand, the rainfall in autumn still brings the MPs from the
(about July). At the end of the simulation, the MPs abundance in land into the water body and increases the abundance of the MPs in the
water decreased compared to the initial value. It may due to some aquatic organisms. On the other hand, the MPs accumulated in aquatic
part of MPs settled into the sediment, and the others were digested organisms cannot be discharged off their bodies quickly. The MPs abun-
and absorbed by aquatic organisms although rainfall brings MPs from dance in aquatic organisms in winter was accordance to that in autumn
land to water. The variation of MPs abundance in detritus indicated or slightly declined. This is because it snows in winter and there is little
that the MPs abundance in detritus increased at the end of simulation, MPs flowing from land to water and the MPs abundance in water is de-
and the abundance of MPs in detritus varies periodically with the annual creased. The MPs in aquatic organisms mainly accumulates in summer

(a) In water (b) Detritus


Fig. 3. The variation of MPs abundance with respect to time in water environment.

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

and autumn and it can't discharge into water quickly as soon as it enters 2020b). This means that the accuracy of formula adopted was high
the winter. and the estimation of the MPs abundance in Baiyangdian Lake is more
reliable.
4.2.3. Time delay of MPs accumulation at different trophic levels Xia et al. (2020) found that the abundance of MPs in Lake Donghu of
In order to detect the delay effect of MPs accumulation in different China increased significantly by analyzing the measured data after rain-
trophic levels, we divided the organism groups in Baiyangdian Lake fall. The relationship between rainfall and the increase of MPs in water
into four trophic levels according to the principle of Lindeman (1942) body was fitted. The fitting formula with R2 = 0.942 is very reliable,
as: first trophic level (detritus), second trophic level (grass carp), third which proves that there is a strong positive correlation between the in-
trophic level (mandarin fish, common carp, crucian carp, chub, fingerling, crease of MPs in water and rainfall. However, the relationship between
mollusc, microzoobenthos, zooplankton) and fourth trophic level rainfall and the increase of MPs abundance in water shouldn't be appear
(snakehead). Fig. 7 showed the delay effect of MPs accumulation in dif- in a linear relationship since there is an upper limitation of the abun-
ferent trophic levels in two periods: beginning simulation period and dance of MPs on land surface. Therefore, we refitted the empirical for-
final simulation period. It was found from Fig. 7(a) that the time of the mula into logarithmic function, which is more consistent with the
MPs abundance in first, second, third, fourth trophic level reached actual situation. The empirical formula was suggested to estimate the
peak value of body MPs abundance was in Sept. 2009, Aug., 2009, MPs abundance of water in densely populated area. Graham et al.
Sept. 2009 and Jan, 2010, respectively. The time of the second trophic (2020) also measured MPs abundance in water and rainfall in Taiwan.
level (grass carp) reached the peak value earlier than that of the first tro- However, the research didn't generate an empirical formula of the rela-
phic level (detritus) because the second trophic level organisms major tionship between the increase of MPs in water and rainfall. According to
feed by submerged plant (exist in bottom of water) and phytoplankton the analyzing method proposed in Xia et al. (2020), we generated the
(exist in surface water). Many MPs in water were majorly distributed empirical formula which is suitable to estimate the MPs abundance of
in surface water (small particle size) and on the bottom of water water in sparsely populated area.
(large particle size). Phytoplankton attaches to MPs on the surface and From the results of Ecopath, it was found that Baiyangdian Lake eco-
it has high MPs abundance. Therefore, the MPs abundance in the second system was dominated by major economic fish common carp, crucian
trophic level (grass carp) reached the peak value earlier than that of the carp, chub and grass carp which contributed the majority of biomass of
first trophic level (detritus). The MPs abundance in the third and fourth 19.2, 134.4, 9.6 and 9.6 t/km2, respectively. The feature of food web
trophic level showed an obvious time delay of MPs abundance. The time structure includes distinctive trophic flow pattern and the correspond-
delay of MPs abundance from the second trophic level to the third tro- ing ecological transfer efficiency (TE) between trophic level (TL). The
phic level and that from the third trophic level to the fourth trophic average TE of the aggregated food chain was estimated at 10.5% which
level are about 17 days and 43 days, respectively. was similar to 10.85% of the immature ecosystem of Sanggou Bay (Sun
For the final simulation period, the response of aquatic ecosystem to et al., 2020).
the abundance of MPs in water has entered a relatively stable period For the ecosystem properties in Table 7, the value of TPP/TR was
after six years development (from 2009 to 2015). Fig. 7(b) showed 2.903, it indicated that the ecosystem of Baiyangdian Lake was a devel-
that the unobvious time delay difference of MPs abundance of the sec- oping ecosystem and the functional groups had more production than
ond trophic level from that that of the third trophic level. This may be respiration. Compared with the results of Tai Lake (Li et al., 2014) and
due to the third trophic level feeds on many groups (detritus and Chao Lake (Liu et al., 2014), Baiyangdian Lake showed a much lower
plants) rather than only feed on the second trophic level (grass carp) TPP/TR value of 4.215. This may indicated that Baiyangdian Lake ecosys-
and this reduces the time delay effect of MPs abundance of the third tro- tem has less aquatic products, and of which most are in the ecosystem
phic level. The delay time difference of MPs abundance of the third tro- recycle while a small part is caught. CI is the ratio between the number
phic level from that of the fourth trophic level was also found in the final of trophic relationships and the total number of possible trophic rela-
simulation period, which was about 17 days. tionships in the system. In Baiyangdian Lake ecosystem, the value of
CI = 0.201 was much smaller than 1 (maturity) and this may due to
5. Discussions the lack interactions of predators and species reduced by human inter-
vention. The SOI quantifies the distribution of feeding interactions
Many studies have found that rainfall and human activities have a among trophic levels of food web through the weighted average of om-
great impact on the abundance of MPs in water (Feng et al., 2020; Liu nivore of consumers. In Baiyangdian Lake, SOI was 0.111, which is rela-
et al., 2020; Xia et al., 2020). Feng et al. (2020) considered two kinds tively higher compared to the Integrated Multi-Trophic Aquaculture
of variables of human activities (night light index and industry output ecosystems in the range of 0.041–0.092 (Li et al., 2014; Liu et al.,
values) which influence the abundance of MPs in water to generate 2014; Sun et al., 2020).
the relationship between human activities and MPs abundance in The differences between these ecosystems and our model results
water. However, there still has a problem since night light index can might be explained by food web by that relatively natural environment
only present the number of families, but it cannot really reflect the num- are usually more complex. It also showed that human interference is
ber of people in a family. Furthermore, families have different lighting high in Tai Lake, Chao Lake and Sanggou Bay compared to Baiyangdian
times and night light index hardly reflects all families. For these reasons, Lake. Since the maturity and stability of Baiyangdian Lake is low and it
the night light index is not a good variable to present the influence of is more susceptible to human activities, it is important and meaningful
human on abundance of MPs. Furthermore, the empirical formula of to detect the effect mechanism of pollutants, such as MPs on the ecosys-
Feng et al. (2020) has an obvious error that with the increase of industry tem of Baiyangdian Lake.
output value, the MPs in water is decreased. In our opinion, the abun- Previous studies have found that MPs widely exist in aquatic organ-
dance of MPs in water should be increased with the increase of industry isms (Von et al., 2012; Fleurine et al., 2020; Tu et al., 2018). However,
output or population. Therefore, the coefficients of empirical formula the research on trophic transfer mainly focuses on the isolation effect
should be all positive number. of MPs in labs, and the description of real-world scenarios is not accu-
For the approach of Xia et al. (2020), they didn't consider the impor- rate enough (Santana et al., 2017; Carbery et al., 2018). How the abun-
tant variable rainfall which was proved to be the important variable de- dance of MPs in aquatic organisms with respect to time and the
termining the process of MPs from land to water. In this research, the mechanism of accumulation through food webs under natural condition
results combined human activities (local GDP and industrial output of is still not clear.
fiber and plastics) with annual rainfall to generate the empirical formula In our research, we selected Baiyangdian Lake as research area and
to estimate the MPs abundance in water was adopted (Ma and You, analyzed the abundance of MPs in aquatic organisms with respect to

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

time and the mechanism of accumulation through food webs. It was human exist in the highest trophic level in nature, the abundance of
found that the MPs abundance in environment and aquatic organisms MPs accumulated in human body through food web will be very high,
is in a periodic change corresponding to rainfall intensity and reaches and a large number of MPs will harm human health. This inference is
a peak in the summer of each year. At the end of 8-year simulation pe- consistent with the viewpoint of Wang et al. (2019). Therefore, we
riod, the accumulation degree of MPs in different aquatic organisms was should pay more attention to the effects of MPs on human and aquatic
different and it was about 1.48–3.97 times of their initial abundance. organisms.
The highest trophic level snakehead had the highest accumulation de- Our research demonstrated that the Ecotracer is a capable tool for
gree of MPs, which reached 3.97 times of the initial abundance. Since tracing MPs through all functional groups of ecosystem, which requiring

(a) Snakehead (b) Mandarin fish

(c) Common carp (d) Crucian carp

(e) Chub (f) Fingerling


Fig. 4. The variation of MPs abundance (×1010 items) with respect to time in aquatic organisms.

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

(g) Grass carp (h) Mollusc

(i) Zooplankton (j) Microzoobenthos


Fig. 4 (continued).

relatively few toxicologic input parameters to follow food web flow of The research area selected is an inland water, and the immigration of
contaminant through all levels of ecosystem. Significantly, our approach aquatic organisms was not considered. If the study area is a sea, the im-
also lends itself to the investigation of other contaminants with signifi- migration of aquatic organisms should be considered.
cant impacts on global ecosystems and human health. We suggested Hydrodynamic factors such as velocity and flow direction may have
that further research of applying Ecotracer to study the change of MPs a great impact on the enrichment of MPs in food web. However, Ecopath
in aquatic ecosystems is urgently required. It can be applied to predict model is a mass balance model, which can't take into account the hydro-
the abundance and toxicity of MPs in the ecosystem through food dynamic effect. How to consider the effects of hydrodynamic factors on
webs. In addition, human beings can be added to ecosystem compo- the enrichment of MPs in food web should be studied in the future.
nents to analyze the impact of MPs on human beings through What's more, eutrophication is a kind of water pollution caused by
food webs. excessive content of nitrogen, phosphorus and other plant nutrients. It
In addition to the negative effects, Taipale et al. (2019) demon- often appears in lakes, reservoirs, estuaries, bays and other slow flowing
strated that aquatic micro-organisms can produce, biochemically up- waters. Eutrophication should be also combined with MPs pollution to
grade, and trophically transfer nutritionally important biomolecules study the effects of both on food web and aquatic organisms.
from PE-MPs. This provides a direction for us to re-understand the influ-
ence of MPs. 6. Conclusions
The limitations and the implications for future research should be
outlined. Due to the limitation of data, some parameters were citied The present study is perhaps the first one that seek to detect the var-
from other similar research areas which have similar food web structure iation of MPs abundance with respect to time in aquatic organisms and
(Lars-Henrik et al., 2016; Jabeen et al., 2017; Jiang et al., 2020; Sun et al., environment under nature condition. By analyzing the measured MPs
2018; Tu et al., 2018; Li et al. (2020a, 2020b); Zhou et al., 2020). In the abundance and rainfall data, we generated an empirical formular to es-
follow-up study, the measured data of the study area should be ob- timate the MPs inflow in water. Combined with the abundance of MPs
tained through experiments to further verify the reliability of the model. in aquatic organisms and other parameters obtained by the measured

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

Fig. 5. The abundance of MPs (×1010 items) in aquatic organisms before (2009) and after the simulation (2016).

data in other research areas with similar ecosystem structure, the vari- throughput was 17,905.961 tkm−2a−1. It showed that Baiyangdian
ation of MPs abundance in aquatic organisms and environment under Lake was in immature stage in 2009, which may more vulnerable to
nature condition was studied by Ecopath and Ecotracer models. human activities (MPs pollution).
Based on results of Ecopath in 2009, it was concluded that the TL of For the ecosystem properties in Baiyangdian Lake, the value of TPP/
major economic fishes is 2.161–2.347 with an average TL of 2.286. TR, CI and SOI was 2.903, 0.201 and 0.111, respectively. The values of FCI
Transfer efficiency in Baiyangdian Lake ecosystem was 10.5%. The sum and FMPL were 2.926% and 4.727%, respectively. All the above indicators
of all production was 8671.14 tkm−2a−1 and the total system showed that the ecosystem of Baiyangdian Lake was a developing

Fig. 6. The variation of MPs abundance (×1010 items) in aquatic organisms in four seasons of 2015.

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Y. Ma and X. You Science of the Total Environment 762 (2021) 144110

(a) Initial simulation period (b) Final simulation period


Fig. 7. The delay effect of MPs accumulation in different trophic levels in two periods.

ecosystem and the minimization disturbance of human was suggested to be of global concern as long as there are ongoing anthropogenic in-
to protect the ecosystem. puts of MPs. The present ecosystem-scale simulation demonstrates the
From the results of Ecotracer, it was found that the MPs abundance enrichment effect of MPs through food web is obvious. Since human-
in environment and aquatic organisms showed a periodic change with beings is the highest nutritional level in nature, we can expect that
rainfall intensity and reached a peak in the summer of each year. The ac- MPs largely accumulate in human body and eventually affect people's
cumulation degree of MPs in aquatic organisms was different, which health. Further research should be focused on the accumulation and
was about 1.48–3.97 times of the initial abundance. The highest trophic toxicity of MPs enriched through food webs.
level snakehead had the highest accumulation degree of MPs, which was
3.97 times of the initial abundance. In terms of seasons, there are rela- CRediT authorship contribution statement
tively low MPs in aquatic organisms in spring, so it is better for people
to choose more aquatic products in spring. Human is in the highest tro- Yi-fei Ma: Conceptualization, Methodology, Software, Writing –
phic level in nature, the abundance of MPs accumulates in human body original draft, Data curation, Writing – review & editing. Xue-yi You:
through food web is high, and a large number of MPs harm human Conceptualization, Writing – review & editing.
health. Therefore, we should pay more attention to MPs accumulation
in human body and ecosystems.
Our research also found the time delay effect of MPs abundance at Declaration of competing interest
different trophic levels. In general, the higher the nutrient level is, the
more obvious the delay effect of MPs accumulation between trophic The authors declare that they have no known competing financial
levels is. interests or personal relationships that could have appeared to influ-
This study provided a reference of further research on the cumula- ence the work reported in this paper.
tive effects of MPs through food webs in ecosystems. MPs will continue
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