Microplastics in aquatic environments: Toxicity to trigger ecological consequences

Journal Pre-proof Microplastics in aquatic environments: Toxicity to trigger ecological consequences Ma Hui, Pu Shengyan, Liu Shibin, Bai Yingchen, Sandip Mandal, Xing Baoshan PII:

S0269-7491(19)35364-3

DOI:

https://doi.org/10.1016/j.envpol.2020.114089

Reference:

ENPO 114089

To appear in:

Environmental Pollution

Received Date: 18 September 2019 Revised Date:

20 January 2020

Accepted Date: 27 January 2020

Please cite this article as: Hui, M., Shengyan, P., Shibin, L., Yingchen, B., Mandal, S., Baoshan, X., Microplastics in aquatic environments: Toxicity to trigger ecological consequences, Environmental Pollution (2020), doi: https://doi.org/10.1016/j.envpol.2020.114089. 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. © 2020 Published by Elsevier Ltd.

1‐

Microplastics in Aquatic Environments: Toxicity to Trigger

2‐

Ecological Consequences

3‐

4‐

Ma Hui 1, 2, Pu Shengyan1, 3, 4,*, Liu Shibin1, Bai Yingchen3, Sandip Mandal1,

5‐

Xing Baoshan4 1

6‐

State Key Laboratory of Geohazard Prevention and Geoenvironment Protection

7‐

(Chengdu University of Technology), Chengdu 610059, Sichuan, China; 2

8‐

Department of Plant and Environmental Sciences, University of Copenhagen,

9‐

Thorvaldsensvej 401871 Frederiksberg, Denmark 3

10‐

State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese

11‐

Research Academy of Environmental Sciences, Beijing 100012, China 4

12‐

Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA 01003,

13‐

United States

14‐ 15‐

Abstract

16‐

The prevalence of microplastic debris in aquatic ecosystems as a result of

17‐

anthropogenic activity has received worldwide attention. Although extensive research

18‐

has reported ubiquitous and directly adverse effects on organisms, only a few

19‐

published studies have proposed the existence of long-term ecological consequences.

20‐

The research in this field still lacks a systematic overview of the toxic effects of

21‐

microplastics and a coherent understanding of the potential ecological consequences.

22‐

Here, we draw upon cross-disciplinary scientific research from recent decades to 1)

23‐

seek to understand the correlation between the responses of organisms to

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microplastics and the potential ecological disturbances, 2) summarize the potential ‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐‐ Corresponding author at: State Key Laboratory of Geohazard Prevention and Geoenvironment Protection (Chengdu University of Technology), Chengdu 610059, PR China. Tel./fax: +86 (0) 28 8407 3253; E-mail: [email protected]; [email protected] (S.Y. Pu); [email protected](B. Xing) Notes: The authors declare that there is no conflict of interests regarding the publication of this paper.

*

1‐ ‐

25‐

ecological consequences triggered by microplastics in aquatic environments, and 3)

26‐

discuss the barriers to the understanding of microplastic toxicology. In this paper, the

27‐

physiochemical characteristics and dynamic distribution of microplastics were related

28‐

to the toxicological concerns about microplastic bioavailability and environmental

29‐

perturbation. The extent of the ecological disturbances depends on how the

30‐

ecotoxicity of microplastics is transferred and proliferated throughout an aquatic

31‐

environment. Microplastics are prevalent; they interfere with nutrient productivity and

32‐

cycling, cause physiological stress in organisms (e.g., behavioral alterations, immune

33‐

responses, abnormal metabolism, and changes to energy budgets), and threaten the

34‐

ecosystem composition and stability. By integrating the linkages among the toxicities

35‐

that range from the erosion of individual species to the defective development of

36‐

biological communities to the collapse of the ecosystem functioning, this review

37‐

provides a bottom-up framework for future research to address the mechanisms

38‐

underlying the toxicity of microplastics in aquatic environments and the substantial

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ecological consequences.

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Keywords: Microplastics; toxic effects; aquatic environment; ecotoxicology

41‐

Table of Contents

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1. Introduction ......................................................................................................................................3

43‐

2. Clues from microplastic features: bioavailability and toxicity determined by

44‐

physiochemical properties ....................................................................................................................4

45‐

3. Spatial and temporal dynamics (distribution) affects the microplastic ingestion by

46‐

organisms............................................................................................................................................13

47‐

4. How will the organisms respond to the microplastic toxicity ........................................................17

48‐

5. What ecological consequence will be triggered by the microplastic disturbance?.........................22

49‐

6. The contradictory opinions for the microplastic toxicity & future research perspective ...............27

50‐

Acknowledgments .............................................................................................................................30

51‐

References ..........................................................................................................................................40

52‐ 53‐ 54‐ 2‐ ‐

55‐

1. Introduction

56‐

Plastic has become a major commodity in the modern world on an unprecedented

57‐

global scale, penetrating basically every aspect of our lives. The plastic industry

58‐

expands annually, but the consumption needs have not appeared to decrease. The total

59‐

plastic production has been estimated to reach 33 billion tons by 2050 [1]. Because

60‐

plastic is a persistent synthetic polymer, scientists started to question where all the

61‐

discharged plastic debris had gone [2]. Microplastics, which have been reported

62‐

sporadically since as early as the 1970s, are now believed to be the predominant form

63‐

of discharged plastic waste [2] and have generated considerable research interest since

64‐

2004 [3]. The disappearance of plastics suggests not only that the small plastic

65‐

particles from cosmetics, clothing and other industrial manufacturing is entering into

66‐

the aquatic environment directly (as primary microplastics) but also that the abundant

67‐

microplastics are generated from the breakdown of large plastic debris in the form of

68‐

plastic fragments, fibers, and granules (as secondary microplastics) [4, 5]. The

69‐

recognition of microplastics as a globe issue was raised from the detection of

70‐

microplastics worldwide [6, 7]. Efforts have been made to develop advanced sampling

71‐

and analytical techniques with higher accuracies in the wake of the increased research

72‐

[4, 8, 9]. After the development of these techniques, signs of stress were observed in

73‐

organisms as a result of microplastics [10-12]. Because of their small size and

74‐

ubiquity, the microplastic particles that have spread in aquatic [13, 14], terrestrial [15]

75‐

and atmospheric [16, 17] environments have high bioavailability for different species.

76‐

Evidence of microplastics has been found in the guts of benthic invertebrates, fish

77‐

[18], and larger mammals [19] from different trophic levels, and the ingested

78‐

microplastics are transferred throughout the food web, driving increasing concerns

79‐

about the threats to aquatic biota [10, 20]. Both direct and indirect evidence for the

80‐

adverse effect of microplastics have been found as a result of the interference with

81‐

fecundity and mortality and the dosage-effect relationship with physiological stress,

82‐

including behavioral alterations [21], immune responses [22], abnormal metabolism

83‐

[23], and changes in energy budgets [24].‐ 3‐ ‐

84‐

We present this particular review because, whereas the negative effect of

85‐

microplastics on organisms and the environment have been widely reported, the

86‐

potential indirect impacts on the ecosystem have received less attention, and few

87‐

published results have proposed long-term ecological consequences. However, the

88‐

question of whether the interference of microplastics is truly harmful has never been

89‐

addressed due to the ambiguous results obtained from nonstandardized research

90‐

methods and the complexity of aquatic ecosystems [25]. A comprehensive comparison

91‐

of the scattered results would be beneficial for developing a sound and overarching

92‐

framework for an improved understanding of microplastics as an anthropogenic

93‐

change in this new epoch. In this review, the most discussed physiochemical

94‐

characteristics were summarized from the perspective of the reasons that widely used

95‐

plastics become toxic pollution the aquatic environments in the form of microplastics.

96‐

By systemically summarizing the diverse toxicological effects of microplastics, the

97‐

links between the superficial phenomena and the in-depth toxicological mechanisms

98‐

were established to advance the knowledge of the potential long-lasting ecological

99‐

threats to the aquatic ecosystem, providing a comprehensive framework and guidance

100‐

for future research. In addition, the most recent research gives recommendations for

101‐

the definition of microplastics [26], but considering the nonstandardized methods in

102‐

the studies in last decade, this review chose the most frequently used definition to

103‐

encompass the largest range of microplastics, which are those under the size of 5000

104‐

µm, without further differentiation of the specific textures, shapes or compositions [27,

105‐

28].

106‐

2. Clues from the features of microplastics: bioavailability and

107‐

toxicity are determined by the physicochemical properties

108‐

In toxicological studies, the physicochemical properties of microplastics are

109‐

provided as the fundamental information, which reflects the focus of the research.

110‐

However, the inherent nature of microplastics is also related to their bioavailability

111‐

and toxicity in aquatic environments. Therefore, instead of describing the

112‐

physiochemical properties in detail, efforts will be made in this review to reveal the 4‐ ‐

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influence on the ingestion preferences and biological responses of different species

114‐

and the profound ecological implications.

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2.1. Physical property

116‐

Bioavailability, which is the key factor reflecting the potential influence of

117‐

microplastics on different species, depends on both the properties of the pollutant and

118‐

the foraging preferences of the organisms [29]. Unlike most selective forgers,

119‐

organisms exhibiting generalist feeding preferences and prey capture methods (e.g.,

120‐

predators only distinguish food from other substances based on limited characteristics)

121‐

are more likely to ingest microplastics with similar features to their natural prey [30].

122‐

Physical properties affect the morphology and mobility of microplastics within the

123‐

aquatic environment, which affects bioavailability by altering the distribution within

124‐

the aquatic environment, presenting a similar appearance to natural substances and

125‐

causing different extents of physical damage to the organism. The most studied

126‐

physical properties include the size, color, density and shape of microplastics, and

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each of the properties contributes differently to the negative effects.

128‐

Size

129‐

Microplastics occupy the same size range as sand grains, microalgae and

130‐

plankton, which are available to a wide range of aquatic organisms, especially the

131‐

nonselective foragers [31]. The microplastic uptake rate by Daphnia magna has been

132‐

shown to have an exponential correlation with size, and the number of daphnids with

133‐

microplastics in their guts decreases with the increase in the average particle size [32].

134‐

The most frequent size of microplastic ingested by daphnids was shown to be below

135‐

100 µm, which is consistent with the food size preference of daphnids [32]. Compared

136‐

to daphnids, Artemia franciscana was shown to ingest fewer microplastic particles

137‐

under the same microplastic exposure conditions due to its smaller food feeding

138‐

preferences (< 50 µm) [33]. For the amberstripe scad Decapterus muroadsi

139‐

(Carangidae) fish, the most commonly ingested microplastics are similar in size to

140‐

their prey, at approximately 1.3 ± 0.1 mm [34]. After ingestion, the particle size is a

141‐

crucial factor determining the translocation ability of microplastics within the body of

5‐ ‐

142‐

an organism. The smaller microplastics (~3.0 µm) translocate within Mytilus edulis

143‐

more easily and readily than the larger particles (~9.6 µm) [35]. The translocation of

144‐

microplastics from the digestive tracts to other tissues within the brown shrimp

145‐

Crangon crangon (L.) was negligible when the particle size was larger than 20 µm

146‐

[36]. Thus, for this specific species, the smaller microplastics showed higher

147‐

bioavailability due to the higher ingestion rate and the translocation rate within the

148‐

organism. On the other hand, for different species, the biological responses also varied

149‐

with the diverse food size preferences and the body size of the organisms. For

150‐

instance, the 0.05 µm microplastics caused the highest toxicity for the monogonont

151‐

rotifer Brachionus koreanus because smaller microplastics have higher retention times

152‐

and thus can exert negative effects due to low egestion efficiency [37]. For

153‐

Caenorhabditis elegans, the 1.0 µm particles caused the highest lethality, maximum

154‐

accumulation, lowest Ca2+ level in the intestine and highest expression of glutathione

155‐

S-transferase 4 compared to both the larger (0.1 µm) or smaller (5.0 µm) microplastics

156‐

since the 1 µm microplastic induced severe intestinal damage [38]. The general

157‐

pattern of differing impacts of different microplastics sizes for different species

158‐

remains unclear, yet the bioavailability of microplastics is affected by the diverse

159‐

morphologies and physiological structures of organisms, which are directly related to

160‐

the ingestion likelihood, egestion rate and translocation potential. Therefore, precise

161‐

model organisms should be selected for toxicological studies based on the aims of the

162‐

research. It is also noteworthy that the controlled microplastics of uniform size that

163‐

are used in research do not align with the sizes in the actual aquatic environment. The

164‐

voluntary food intake behavior of organisms should be considered by exposing

165‐

organisms to a wider ranges of microplastic sizes. The comprehensive consideration

166‐

of both the range of microplastic sizes in the aquatic environment and the features of

167‐

the native species is critical for obtaining reliable results during ecotoxicological tests

168‐

or risk assessments.

169‐

Color Color is another aspect of microplastics that disturbs foraging by visual predators

170‐

6‐ ‐

171‐

with various ingestion biases. For instance, 80% of the amberstripe scads (Decapterus

172‐

muroadsi) in a previous study ingested mainly blue polyethylene fragments, which

173‐

presented a similar morphology in color and size with their blue copepod prey (Fig. 1)

174‐

[34]. Mostly dark colors of microplastics, especially green microplastic fibers, which

175‐

resembled marine plankton, were found in the digestive systems of flathead grey

176‐

mullet Mugil cephalus [39]. The white, clear and blue microplastics, which are similar

177‐

in color to the plankton in the area, were the most common colors of the microplastics

178‐

ingested by the planktivorous fishes in the North Pacific central gyre due to the

179‐

resemblance to the food source of the fish [40]. Thus, the ingestion propensity of

180‐

visual predators is significantly affected by the color of microplastics.In addition to its

181‐

impact on the ingestion preferences, the color of microplastics was also studied as an

182‐

intuitive indicator reflecting the potential toxicity of microplastics. The enrichment of

183‐

PAH in microplastics composed of polyethylene and polypropylene showed no

184‐

difference, while a predictable increase in the PAH concentration was observed along

185‐

with the darkening of the color [41]. Moreover, the lighter colored microplastics are

186‐

prone to having lower molecular weight PAH, and darker microplastics contain higher

187‐

weight PAH [41]. This difference in adsorption capacity due to color also revealed

188‐

that the black microplastics tended to adsorb more chemicals, such as PCBs and PAHs,

189‐

than the white ones [42]. As a result, the organisms would have the additional stress of

190‐

enriched contaminants throughout the circulatory system, tissues and organs due to

191‐

ingestion along with the microplastics. One possible reason for these color-related

192‐

results could be that different pigments are beneficial to the adsorption capacity of

193‐

microplastics [43]. Additionally, the color could reflect the relative age and degree of

194‐

weathering of the microplastic. The affinity between the microplastic surfaces and

195‐

contaminants is affected, and the loss of the pollutants on the surface of the

196‐

microplastic during weathering results in a low degree of adsorption. The direct

197‐

relationship between color and pollutant enrichment is a very new finding in

198‐

toxicological research. The underlying mechanisms from the aspects of the chemical

199‐

composition and how the microplastics with different colors behaved in the aquatic

7‐ ‐

200‐

environment should be studied. Moreover, considering the ingestion preference of the

201‐

organisms and the predictable variation of the contaminant enrichment, monitoring of

202‐

the microplastic color spectrum could be beneficial to the preliminary assessment of

203‐

microplastic toxicity for organisms with different feeding preferences.

204‐

Density

205‐

Density influences the distribution and destination of microplastics by affecting

206‐

the trajectory, sinking velocity and spatial distribution of microplastics, which further

207‐

affects the microplastic distribution in the different biota and habitats. For instance,

208‐

the spread of low-density plastics over the surface water impedes the photosynthesis

209‐

of the algae and the respiration of the zooplankton [44], high-density microplastics

210‐

have been consistently detected in the digestive tracts of the benthic invertebrates [45,

211‐

46], and the microplastics that sink to the sediments on the seafloor endanger the deep

212‐

ocean biota [47].

213‐

Moreover, the low-density microplastics ingested by copepods from the surface

214‐

water are excreted in a mixture with the feces after digestion. The density change

215‐

alters the sinking velocity of the copepod-egested fecal pellets, which are important

216‐

food sources for fish, polychaetes, crustaceans and copepods. Consequently, the food

217‐

distribution for marine organisms may be impacted, and the bioavailability of

218‐

microplastics is aggravated during feeding [48]. Furthermore, contaminants such as

219‐

polycyclic aromatic hydrocarbons [49], polychlorinated biphenyls [50], and

220‐

phenanthrene [51] tend to have higher diffusion coefficients in low-density

221‐

microplastics than in high-density microplastics, which directly affects microplastic

222‐

toxicity. Therefore, the density of microplastics in further toxicological studies should

223‐

be considered to be a property with the potential for 1) altering the exposure pathway

224‐

of the contaminants along with the microplastics, 2) inducing combined toxicity

225‐

effects with other pollutants, and 3) causing ecological turbulence by disturbing the

226‐

distribution of food in the aquatic environment.

227‐

Shape The shape of microplastics is a critical morphological feature that has been

228‐

8‐ ‐

229‐

generally divided into regular and irregular shapes considering the initial shape and

230‐

the aging and weathering conditions. More specifically, microplastics can also be

231‐

classified as spheres, fibers, fragments, pellets, films, and flakes [52]. The shape alters

232‐

the hydrodynamic characteristics of microplastics, which relates to a series of

233‐

biological and toxicological effects by disturbing the distribution and bioavailability.

234‐

Unlike density, shape affects the dynamics of microplastics indirectly. The settling

235‐

velocity of microplastics in aquatic environments varies due to their varying shapes

236‐

[53]. Plastic fibers and thin films show higher buoyancy and lower settling velocity

237‐

than spherical plastic particles even if the debris have the same density and volume

238‐

[54, 55]. Based on simplified physical models and geometrical considerations, the

239‐

transport times of polystyrene microplastics in the aquatic environment follow the

240‐

order of foamed polystyrene
241‐

Since the predation processes of most aquatic organism are also dynamic, the changes

242‐

in the microplastic settling and eventual fates due to different morphological shapes

243‐

indirectly affect the opportunities for ingestion and the bioavailability.

244‐

After ingestion, the shape of the microplastics also affects the egestion and

245‐

residence time within the body. For example, D. magna rapidly ingests both regularly

246‐

and irregularly shaped polyethylene microplastic particles, but the gut clearance and

247‐

apparent gut residence times of the irregular microplastic particles were longer than

248‐

those for the irregularly shaped microplastic particles and were even accompanied by

249‐

more pronounced acute inhibitory effects [57]. The microplastic fibers ingested by the

250‐

amphipod Hyalella azteca required longer clearance times than the spheres, and

251‐

higher toxicities were found for the microplastic fibers, which were attributed to

252‐

longer residence times because of the shape [58]. Discharged plastic debris with the

253‐

same composition behaves differently in the aquatic environment, and the threats

254‐

caused by irregularly shaped microplastics tend to be higher due to the difficulty of

255‐

egestion and clearance for organisms compared to the regular spherical particles.

256‐

2.3. Chemical properties

257‐

The chemical nature of microplastics is determined by the plastic composition and

9‐ ‐

258‐

synthesis methods and is expressed as various chemical characteristics, such as

259‐

different functional groups, surface polarities, stabilities, and crystallinities, which

260‐

enable the identification of the microplastics with the potential to leach additives from

261‐

particles or to accumulate environmental pollutants on the surface. Unlike the

262‐

physical properties that directly affecting ingestion or egestion or cause physical

263‐

injury to organisms, the chemical properties of microplastics are related to their

264‐

persistence affinity for chemicals. The patterns of enrichment with contaminants and

265‐

the release of additives change with the prevalence of microplastics; thus, the changes

266‐

in the behavior of the microplastics are discussed from the aspect of the chemical

267‐

properties.

268‐

Functional groups & affinities with pollutants

269‐

The functional groups and polarities of microplastics contribute the most to the

270‐

accumulation of contaminants from the ambient environment (Fig. 2.). The partition

271‐

coefficient Kd of perfluorooctanesulfonamide (FOSA) with different microplastics

272‐

follows

273‐

(Kd(PVC)=115.7 L/kg)>polystyrene (Kd(PS)=84.9 L/kg). The highest Kd for the nonpolar

274‐

PE has been attributed to the strong hydrophobic affinity between the microplastic

275‐

and the symmetric nonionic FOSA. The benzene rings on PS cause steric hindrance of

276‐

the bond rotation and decrease the free volume between the chains, leading to the low

277‐

sorption levels [59]. The adsorption of the antibiotics sulfadiazine (SDZ), amoxicillin

278‐

(AMX), tetracycline (TC), ciprofloxacin (CIP) and trimethoprim (TMP) on the 5

279‐

types of microplastic polyethylene (PE), polystyrene (PS), polypropylene (PP),

280‐

polyamide (PA), and polyvinyl chloride (PVC) depends on the hydrogen bonding,

281‐

hydrophobic interaction, van der Waals forces and electrostatic interactions, and the

282‐

highest adsorption capacity of PA with antibiotics is attributed to the strong

283‐

H-bonding with the amide groups [60]. The adsorption behavior of polyethylene (PE),

284‐

polystyrene (PS) and polystyrene carboxylate (PS-COOH) with 18 perfluoroalkyl

285‐

substances (PFASs) follows the order PS>PS-COOH>PE, and the influence of the

286‐

hydrophobic interaction between PFASs with microplastics has been shown to

the order of

polyethylene (Kd(PE)=298.3

10‐ ‐

L/kg)>polyvinyl

chloride

287‐

increase the toxicity of hydrophobic contaminants to organisms and aquatic

288‐

ecosystem [61]. In addition to pollutant accumulation, the functional groups on

289‐

microplastics may also directly interfere with microplastic toxicity. For instance, no

290‐

significant difference between the adsorption of Ni on PS and PS-COOH was found,

291‐

yet the toxicity of Ni mixed with PS-COOH was higher than that with PS. The

292‐

detailed mechanism for this phenomenon remains unclear; nevertheless, the combined

293‐

effect suggests that the toxicity of pollutants varies with the different functional

294‐

groups of microplastics [62].

295‐

Crystallinity

296‐

In aquatic environments, the crystallinity of an adsorbent may affect the separation of

297‐

the HOC (hydrophobic organic contaminants) from carbohydrates and other

298‐

semicrystalline (biological) polymers [63]. Organic adsorbents in the environment are

299‐

composed of organic polymers that contain both crystalline and amorphous phases.

300‐

The crystalline areas are categorized by molecules or molecular segments that are

301‐

usually arranged in lattices. In contrast, the amorphous regions have randomly

302‐

arranged molecules, thus showing a loose and flexible structure that is more similar to

303‐

that of a liquid. The adsorption of HOC usually occurs on the amorphous areas due to

304‐

its internal structure, which is characterized as glassy or rubbery. The adsorbent could

305‐

be considered a mixture of glass and rubber polymers. Organic pollutants tend to have

306‐

higher affinities for rubber plastics than for glass plastics [64-66]. The polymer

307‐

portion of the glass phase has higher adhesion and more concentrated force, while the

308‐

polymer segment of the rubber phase shows greater fluidity and flexibility and can be

309‐

thought of as a dynamic viscous liquid. Because of their rigidity, glass polymers have

310‐

a long life and closed internal nanoholes, which can act as adsorption sites for organic

311‐

contaminants in water. The characterization of crystallinity could facilitate further

312‐

assessments of the affinity between microplastics and environmental pollutants.

313‐

Stability

314‐

The additives used during plastic synthesis, such as monomers, oligomers, pigments,

315‐

reinforcements, and plasticizers, usually present high toxicity to organisms. The

11‐ ‐

316‐

weathering alters the properties of microplastics and accelerates the release of some

317‐

superfluous compounds from the microplastics [67], threatening the ecological health

318‐

of aquatic ecosystems. Significant enrichment of hexabromocyclododecanes

319‐

(HBCDDs) has been found in marine sediments and mussels, and the subsequent

320‐

research to identify the source confirmed that HBCDDs were leached from expanded

321‐

polystyrene (EPS), which is a widely used material in aquaculture farming. In

322‐

addition, the acute toxicity of leachates from different plastics varies differently after

323‐

irradiation and weathering. To test the toxicity caused by the low stability, twenty-one

324‐

types of plastic debris were irradiated with artificial sunlight; 38% of these

325‐

microplastics had leachates that resulted in acute toxicity to the marine harpacticoid

326‐

copepod Nitocra spinipes [68]. Both the plastic-derived chemicals bisphenol A (BPA)

327‐

and di-2-ethylhexyl phthalate (DEHP) have been reported to cause 1.2- to 50-fold

328‐

reductions in biomass and to perturb the photosystem and photosynthetic activity of

329‐

the marine toxic dinoflagellate Alexandrium pacificum [69]. Exposure experiments

330‐

with microplastics made from polyethylene terephthalate (PET) and its associated

331‐

plasticizer

332‐

Parvocalanus crassirostris showed that the nauplii were severely impacted even at

333‐

low chemical concentrations, presenting a 48 h LC50 value of 1.04 ng/L. DEHP did

334‐

not show a significant impact on the adult copepods. However, the egg production of

335‐

the copepods was reduced under the sublethal concentration of DEHP or the

336‐

microplastic [70]. This induction of a heritable reproductive disorder by the

337‐

microplastic and its plasticizer poses a potential threat to subsequent generations of

338‐

copepods and even the organisms at higher trophic levels. In addition, not only the

339‐

organic additives but also the release of the total organic carbon, Cl, Ca, Cu, and Zn

340‐

from the aged microplastics were significantly increased due to photooxidation in the

341‐

aquatic environment. New adsorption bands of -C

342‐

during the aging process, which emphasizes the importance of analyzing the stability

343‐

of microplastics during toxicity tracking research and risk assessments [71].

344‐

Surface charge

Di(2-ethylhexyl)phthalate

(DEHP)

12‐ ‐

with

the

calanoid

copepod

O -C—O and -OH were formed

345‐

The surface charge of microplastic has rarely been discussed in comparison with

346‐

the functional groups and the polarity; however, the contribution to microplastic

347‐

toxicity is nonnegligible. The embryotoxicity test of PS-COOH and PS-NH2 for

348‐

embryos of the sea urchin Paracentrotus lividus suggested that the status of the

349‐

charges (i.e., +/-) caused various dispersion patterns of the microplastics inside the

350‐

bodies of the studied organisms, and only PS-NH2 disrupted the cell membrane and

351‐

caused oxidative stress, which eventually induced cell death by apoptosis in the sea

352‐

urchin embryos [72]. The opposite surface charges of microplastics and natural

353‐

organic matter compounds and minerals also facilitate their interactions in aquatic

354‐

environments. The nanoscale materials in natural media are generally charged, and the

355‐

heteroaggregation with microplastics due to opposite surface charges further

356‐

influences the uptake rate by biota and the biodistribution of this nutrient matter,

357‐

disrupting the essential physiological functions linked to the feeding and growth of

358‐

organisms [73, 74]. Both the neutral and positively charged microplastics increased

359‐

TiO2 NP toxicity for the marine algae Chlorella sp., and the oxidative stress followed

360‐

the trend TiO2 NPs+ Plain PS/NH2-PS > TiO2 NPs+ COOH-PS [75].

361‐

3. Spatiotemporal dynamics (distribution) affect microplastic ingestion by

362‐

organisms

363‐

While the pressure of microplastics on aquatic ecosystems is increasingly

364‐

recognized, the understanding of the spatiotemporal dynamics of microplastics

365‐

remains limited. The spatial dynamics reflect the distribution and pollution conditions

366‐

of microplastics, and the temporal dynamics provide information on the fluctuations

367‐

of microplastic contamination over time. The lack of comprehensive consideration of

368‐

the distribution dynamics may lead to biases in contamination monitoring and risk

369‐

assessments. Therefore, the features of the spatiotemporal distribution provide a better

370‐

understanding of the occurrence of microplastics within aquatic ecosystems as well as

371‐

the dynamic toxicity patterns.

372‐

3.1 Spatial distribution The microplastics in aquatic environments travel around the globe, driven by the

373‐

13‐ ‐

374‐

orientation of the coastline and the local wind and wave conditions [17, 76]. An

375‐

annual microplastic survey of three exposed beaches on the Canary Islands proved the

376‐

migration of portable microplastic debris of nonlocal origin from the North Atlantic

377‐

Ocean, driven by the southward-flowing Canary Current [77]. The lateral

378‐

geographical distribution of microplastics in the global ocean far from the polar

379‐

region was reviewed, and the modeling approaches for predicting the fate and

380‐

prevalence of microplastics were summarized [78, 79]. Therefore, in this study, the

381‐

vertical spatial distribution of microplastics in aquatic environments and the

382‐

ecological impact were discussed further.

383‐

According to the distance travelled by sunlight, the ocean is vertically divided

384‐

into the euphotic zone (0~200 m), disphotic zone (200~1000 m), and aphotic zone

385‐

(upon 1000 m) [80]. The phytoplankton, zooplankton, forage fish and predator fish

386‐

are the most affected by the widespread light-weight microplastic in the euphotic zone

387‐

and have been most frequently reported in recent decades. Moreover, the

388‐

accumulation of microplastic particles also occurs within the sea surface microlayer,

389‐

which is the naturally reactive boundary layer between the water and atmosphere [44].

390‐

The accumulated microplastics within the microlayer affect the photochemical

391‐

reactions by interfering with the sunlight irradiation in this region. As a result, the

392‐

photosynthesis, respiration and physiological activities of the plankton are further

393‐

impacted. With the presence of microplastics, the growth of the algae Skeletonema

394‐

costatum has been shown to be inhibited [81], and the roots of a floating plant, the

395‐

duckweed Lemna minor, were mechanically blocked [82]. In addition, the potential

396‐

risk of microplastics acting as a substrate for reactions between complex compounds,

397‐

such as inorganic components, dissolved organic matter, or contaminants enriched in

398‐

the surface microlayer, is another severe issue that may trigger diverse photochemical

399‐

reactions within the euphotic zone.

400‐

The prevalence of microplastics below the euphotic zone mainly depends on the

401‐

diel vertical migration (DVM) of the active mesopelagic fishes that transfer

402‐

microplastics from the sea surface to the disphotic zone and the aphotic zone. The

14‐ ‐

403‐

mesopelagic fishes show a high ingestion rate for microplastics regardless of the

404‐

species, location, or migration behavior, and the movement of mesopelagic fish from

405‐

the euphotic zone to the deep sea mediates the transfer of microplastics to unexposed

406‐

species and regions of the ocean [83, 84]. This phenomenon was further confirmed by

407‐

in situ feeding experiments with the large larvaceans Bathochordaeus, which

408‐

indicated that the microplastics from the sea surface could be delivered to the seafloor

409‐

via biological interference [85]. The ecological consequences are still poorly

410‐

understood, but the unpredictable movement of the mesopelagic fish has facilitated

411‐

the abundant occurrence of microplastics throughout a wide area of the oceans, and

412‐

the further impact on the aquatic ecosystem remains unknown. For the aphotic zone of

413‐

the ocean, microplastics are found ubiquitously on the seafloors of the Southern

414‐

Ocean, North Atlantic Ocean, Gulf of Guinea, and the Mediterranean Sea [86]. The

415‐

microplastics were moved through the ocean and sunk into the deep sediment,

416‐

invading one of the most pristine and vulnerable areas of the marine environment. The

417‐

ingestion of microplastics by lysianassoid amphipods at the deepest location of all the

418‐

Earth’s oceans was detected [87]. The occurrence at the seafloor suggests a long-term

419‐

exposure of benthic ecosystems to microplastics [88].

420‐

3.2 Temporal dynamics

421‐

Seasonal climate change influences the temporal variation in disturbance from

422‐

microplastics. The significant differences in the microplastic amounts sampled from

423‐

Lambra (La Graciosa Island) and Famara (Lanzarote Island) presented seasonal

424‐

occurrence patterns of microplastics in aquatic environments, which is attributed to

425‐

the local-scale wind and the seasonal wave condition variation [77]. In the Pearl River

426‐

in China, the density of plastic debris in the rainy season was reported to be

427‐

significantly higher than that in the dry season because of the larger amount of river

428‐

discharge [89]. The weak management of plastic pollution in inland environments

429‐

allows flooding in urban areas to flush the discharged plastic debris into the ocean. A

430‐

comparison of the microplastic occurrence from December 2016 to January 2017 in

431‐

Mersin Bay suggested that the seasonally heavy rains and floods increased the

15‐ ‐

432‐

microplastic abundance in the aquatic environment over time; after being flushed by

433‐

the floods, the average microplastic size decreased from 2.37 mm (preflood period) to

434‐

1.13 mm (postflood period) [90]. As a consequence of this seasonal occurrence

435‐

pattern, the seasonality of organism assemblages could be threatened by changes in

436‐

the microplastic bioavailability over time.

437‐

The distribution of microplastics, zooplankton and the fish larvae in the

438‐

mangrove creeks of the Goiana Estuary, Brazil, changes with the lunar cycle due to

439‐

the different tidal current regimes. The higher abundance of microplastic threads was

440‐

revealed, while there were fewer zooplankton available in the creeks [91]. Such

441‐

dynamic variation in both the aquatic species and the microplastic occurrence leads to

442‐

seasonal differences and diverse threats to different species. For example, more

443‐

microplastics were detected during summer than spring in the digestive tracts of two

444‐

economically and ecologically crucial planktivorous forage fish, the Atlantic herring

445‐

(Clupea harengus) and the European sprat (Sprattus sprattus), in the Baltic Sea. The

446‐

variation in uptake was mainly due to the seasonal difference in feeding activity,

447‐

which reflected the variation in the vulnerability of the organisms at different

448‐

developmental stages [92]. It is also interesting that zooplanktivores were likely to

449‐

feed on more microplastics than natural prey before the rainy season. Before the rainy

450‐

season, the meroplankton in the macrobenthos could be confused with paint particles,

451‐

whereas styrofoam could be mistaken for immature copepods by predators [93]. The

452‐

possible explanation for this phenomenon could be the lower microplastics abundance

453‐

after the rainy season or the behavioral plasticity for the nonspecific food selection

454‐

ability of the predator.

455‐

The interference of the temporal dynamic of the microplastics tends to be

456‐

complicated and versatile, and the physicochemical parameters and nutritional quality

457‐

of the habitat directly influence the living conditions of the organisms [94]. A better

458‐

understanding of seasonal fluctuations and the subsequent influence induced by the

459‐

microplastics comes from the accuracy and importance of the research. To achieve a

460‐

comprehensive understanding of the ecological disturbance caused by microplastics,

16‐ ‐

461‐

both the spatial and temporal dynamic patterns of microplastics should be considered

462‐

in relation to the seasonal activity of organisms during pollution monitoring,

463‐

toxicological tests, and the subsequent analysis of the instability of ecological health.

464‐

4. How do organisms respond to the microplastic toxicity?

465‐

Many studies have investigated the microplastic-induced adverse effects on

466‐

organisms, which range from disruption of physiological functions to lethal effects.

467‐

Based on the fate of microplastics after ingestion, microplastic toxicity could be

468‐

classified as follows: 1) accumulation within the digestive tract, causing physical damage such as

469‐ 470‐

clogging and injury;

471‐

2) discharge as pseudofeces, which disturbs the energy flow of organisms;

472‐

3) translocation within the body, which exposes the internal tissues and organs to

473‐

microplastics.

474‐

The overall generalization of the microplastic-caused adverse effects on organisms

475‐

was summarized to establish a sound research framework for future microplastic

476‐

toxicological studies and to assess the potential ecological disturbances on a large

477‐

scale.

478‐

4.1 Physical damage

479‐

Physical damage is the most apparent effect from the ingestion of microplastics

480‐

by organisms. The most common damage includes intestinal blockage, cracking of

481‐

villi and splitting of enterocytes [38]. Furthermore, tissue alteration also occurs even

482‐

after the ephemeral occurrence and accumulation. Structural changes in the gills and

483‐

digestive glands, as well as necrosis in other tissues, such as the mantle have been

484‐

observed in mussels after microplastic ingestion [95, 96]. The more detailed and

485‐

specific physical impacts of microplastics were reviewed by Wright et al. [20]. In this

486‐

review, the subtle yet more profound interference with energy storage, metabolism,

487‐

physiological behavior and survival of organisms is further addressed below.

488‐

4.2 Energy budget disturbance Organisms generate false satiation after the ingestion of microplastics, which

489‐

17‐ ‐

490‐

consequently disrupts their regular nutrition and energy intake and leads to abnormal

491‐

physiological responses. Studies of the disturbance of the energy budget caused by

492‐

microplastics have been conducted by monitoring the influence on the ingestion,

493‐

respiration, growth and excretion of the organisms. The filtering activity of the blue

494‐

mussel (Mytilus edulis) was reduced after the ingestion of 100 nm polystyrene

495‐

microplastics, and the feeding activity was further affected [97]. The weight of the

496‐

polychaete worm Arenicola marina was changed by suppressed feeding activity due

497‐

to microplastics, which reflected an up to 50% depletion of the energy reserves [24].

498‐

The ingestion of foods containing microfibers (0.3-1 wt%) by the crab Carcinus

499‐

maenas also reduced the food consumption from 0.33 to 0.03 g/d, and the energy

500‐

available for growth for the crab decreased from 0.59 to -0.31 kJ crab/d [98]. The

501‐

disturbance of the energy budgets of the organisms was always accompanied by the

502‐

production of pseudofeces, and the growth and performance were obstructed as a

503‐

consequence of the reduction in energy intake and depletion of energy reserve

504‐

depletion.

505‐

According to the Wilby 1988 scoring system, the morphology of Hydra attenuate

506‐

also changed significantly after the ingestion of microplastics [99]. The body length of

507‐

Caenorhabditis elegans was significantly reduced after 2 days of microplastic

508‐

exposure due to the decreased energy assimilation [38]. The development of

509‐

Paracentrotus lividus plutei with different body lengths and arm lengths indicated the

510‐

interference of microplastics during postembryonic development; in Ciona robusta,

511‐

metamorphosis was inhibited at an early life stage [100].

512‐

Different species can only function well in an ecosystem when the individual

513‐

organisms maintain healthy physiological states. The ingested and accumulated

514‐

microplastics are transferred to higher trophic levels, and such energy deficiency in

515‐

individual organisms impedes the energy uptake, development and population of the

516‐

species and subsequently disturbs the energy flow through the entire food web [101].

517‐

4.3 Translocation within the body of an organism After ingestion, subsequent microplastic trafficking was observed in different

518‐

18‐ ‐

519‐

organs of organisms, which was followed by gradual yet incomplete renal clearance

520‐

(Fig. 3.). Cytotoxicity research on different nanoparticles suggests that the nature of

521‐

endocytosis and particle-cell interactions provides particles with a pathway to expose

522‐

tissue and organs [102, 103]. After crossing biological barriers (such as cell

523‐

membranes), the microplastics translocated from the digestive system through both

524‐

active and passive physical penetration have a considerable impact on biological

525‐

processes, even causing long-lasting and irreversible damage to organisms [104-107].

526‐

Although the crucial factors for the penetration capability of microplastics remain

527‐

poorly understood, the translocation of microplastics within the body has been shown

528‐

to induce complicated sublethal responses to organisms (Table 1).

529‐

4.4 Metabolism and sublethal responses

530‐

The internal exposure of the circulatory system, tissue and organs to

531‐

microplastics results in metabolic disorders and sublethal responses in organisms,

532‐

which is reflected in endocrine disorders, oxidative stress, immune responses, and

533‐

altered gene expression [108]. The metabolism and growth of an organism are

534‐

simultaneously critically affected by microplastic ingestion. The polystyrene

535‐

microplastics in the guts of the adult zebrafish increased the volume of mucus and

536‐

triggered inflammation after ingestion. The high-throughput sequencing of the 16S

537‐

rRNA gene V3-V4 region and the operational taxonomic unit analysis revealed an

538‐

in-depth response at the phylum and genus levels, suggesting that the microplastic

539‐

exposure within the gut changed the richness and diversity of the microbiota,

540‐

eventually leading to a microbial imbalance [109]. The oxygen consumption of the

541‐

shore crab Carcinus maenas showed a dosage effect from microplastic exposure;

542‐

subsequently, a small but significant decrease in the hemolymph sodium ions and an

543‐

increase in the calcium ions were observed [110]. Another example is that the reactive

544‐

oxygen species (ROS) produced during the phagocytosis of the nanoparticles could

545‐

act as an indicator of cytotoxicity[111]. A significant size-dependent increase in the

546‐

ROS levels in the monogonont rotifer Brachionus koreanus were observed from

547‐

microplastic exposure. The activation of antioxidant-related enzymes as defense

19‐ ‐

548‐

mechanisms further proved the oxidative stress induced by the microplastic [37].

549‐

In further reports, the endocrine system function of the Japanese medaka Oryzias

550‐

latipes was disturbed under microplastic exposure at environmentally relevant

551‐

concentrations, and gene expression was observed to be altered after chronic

552‐

two-month dietary exposure. It is quite relevant that the dosage severely influences

553‐

and regulates choriogenin (Chg H) gene expression in males as well as vitellogenin

554‐

(Vtg I), choriogenin (Chg H) and estrogen receptor (ERα) gene expression in females.

555‐

The histological observation also shows the abnormal proliferation of germ cells in

556‐

one male fish [112].

557‐

Moreover, a transcriptome analysis showed that the microplastic particles were

558‐

integrated into the immunological recognition process of the zebrafish larvae and that

559‐

the nuclear receptors in the lipid metabolism and toxicity pathway were enriched, and

560‐

the colocalization of neutrophils and macrophages was found around the PS particles

561‐

[22]. In another report, a significant neurotoxic effect and oxidative stress was

562‐

observed in the Amphibalanus amphitrite barnacle and Artemia franciscana brine

563‐

shrimp triggered by microplastic accumulation. The low enzymatic activity from the

564‐

damage and the presence of the defense biomarkers cholinesterase (indicative of

565‐

neurotoxicity) and catalase (indicative of oxidative stress) suggested that the

566‐

microplastics disturbed the detoxification of hydrogen peroxide in the organisms [21].

567‐

Underlying the phenomenal inhibitory effect of microplastics on the body length,

568‐

reproduction and survival rates of the nematode Caenorhabditis elegans, the increased

569‐

expression of the glutathione S-transferase 4 enzyme in the intestine suggests that

570‐

intestinal damage and oxidative stress may be the major mechanisms for the toxic

571‐

effects of microplastics [38, 113].

572‐

4.5 The impact on behavioral pattern, fecundity, and survival

573‐

The disruption of behavioral patterns, fecundity and survival are regarded as the

574‐

ultimate toxicological responses of organisms under stress from anthropogenic

575‐

alterations to the environment [114]. The chronic exposure of Ceriodaphnia dubia to

576‐

microplastic fibers had a dose-dependent effect on energy loss and physical damage,

20‐ ‐

577‐

leading to reduced growth and reproduction [115]. In a similar investigation of the

578‐

toxicity and impacts of microplastic, it was observed that the mortality of the Asian

579‐

green mussel Perna viridis was increased due to energy reserve depletion, which

580‐

affected the essential life functions [116].

581‐

Moreover, the abnormal behaviors reflect the distempered physiological functions

582‐

of the organisms, which impact individual development and life survival under harsh

583‐

environmental conditions. The jump height of the beachhopper Platorchestia smithi

584‐

was reduced after ingesting microplastic particles [117]. The swimming activity of

585‐

marine crustaceans was altered under microplastic exposure, and the swimming

586‐

speeds of Amphibalanus amphitrite and Artemia franciscana were inhibited

587‐

significantly due to the mechanical disturbance caused by microplastic agglomeration

588‐

[21]. Similarly abnormal swimming activity was also observed; the water flea C.

589‐

dubia becomes entangled in microplastic clusters, which results in an inability to

590‐

swim [115]. The changes to physiological activity could further interfere with their

591‐

feeding activity and ability to avoid predators.

592‐

Notably, the changes to the behavioral patterns also reflect the subhealthy status,

593‐

potential fecundity interference and the increased mortality of organisms, which

594‐

warns of subsequent ecological effects from the superficial phenomenon. For instance,

595‐

further investigation of the reduction in the jump height of the beachhopper

596‐

Platorchestia smithi revealed that the beachhoppers also suffered from microplastic

597‐

translocation from the gut to the gills. The survival rate was reduced simultaneously

598‐

with the behavioral alternation. Thus, the abnormal behavioral patterns of species

599‐

could act as an indicator of the microplastic burden on the vital activities of organisms

600‐

[117].

601‐

4.6 Combined effects of the inorganic and organic pollutants

602‐

Beyond the direct toxicity caused by microplastics that was discussed above, the

603‐

combined effects of the microplastics and environmental contaminants cause

604‐

worsened contamination. The enduring plastic debris drifting in the aquatic

605‐

environment acts as a reservoir or vector, accumulating widespread trace pollutants,

21‐ ‐

606‐

leading to long-distance transport and high bioavailability of hydrophobic and toxic

607‐

contaminants for organisms. The desorption of chemicals under the conditions in the

608‐

gut is reported to be 30 times higher than that in seawater [118], and the toxicity of

609‐

both the microplastic and environmental pollutants tends to be more detrimental due

610‐

to the combined effects (Table 2). Considering the potential for bioaccumulation and

611‐

biomagnification within aquatic ecosystems, the combined toxicity effects of

612‐

microplastics with different contaminants have been widely studied in recent decades.

613‐

5. What ecological consequence will be triggered by the disturbances from

614‐

microplastics? How is the ubiquity of microplastics related to the function of aquatic ecosystems?

615‐ 616‐

To maintain an intact aquatic environment, different environmental elements and all

617‐

species provide valuable ecological services for the ecosystem. However, by altering

618‐

natural habitats; disturbing the bacterial community; disrupting the development of

619‐

species, populations and communities development; and indiscriminately interfering

620‐

with the indispensable ecological functions of the ecosystem, widespread

621‐

microplastics jeopardize basically every process in an ecosystem. These disturbances

622‐

are known to threaten ecosystem stability, but forecasting the direct outcomes from

623‐

scattered evidence is not yet possible. For an improved understanding of the linkage

624‐

between environmental perturbations and the prevalence of microplastics, identifying

625‐

the distress signals that foretell major disruptions to ecology may one day predict, or

626‐

perhaps even prevent, the potential destabilization of ecosystems.

627‐

5.1 Ecosystem productivity disturbance

628‐

The prosperity of aquatic ecosystems is supported by steady ecosystem

629‐

productivity, and primary production plays a fundamental role in structuring aquatic

630‐

food webs. However, the ubiquity of microplastics as a human-driven environmental

631‐

change may lead to losses in ecosystem productivity by obstructing nutrient

632‐

production and cycling within ecosystems. By using salps as model organisms under

633‐

environmentally relevant concentrations, microplastics were detected in the fecal

634‐

pellets. Under potential future scenarios, up to 46% of fecal pellets are predicted to

22‐ ‐

635‐

contain microplastics, which would lower the efficiency of biological pumps in

636‐

driving sequestration of the anthropogenic carbon in the ocean [119]. Moreover, the

637‐

interactions between the microalgae Skeletonema costatum and microplastics, such as

638‐

adsorption and aggregation, reduce the algal chlorophyll content, resulting in low

639‐

photosynthetic efficiency. The growth of algae has been shown to be inhibited, and

640‐

subsequently, the biomass of this marine primary producer was reduced [81].

641‐

Heteroaggregation was shown to trigger the overexpression of the sugar biosynthesis

642‐

pathways in microalgae [120]. Microplastics have also been widely reported to cause

643‐

the physiological activities of moving and burrowing to be defective in the lugworm

644‐

Arenicola marina, which plays an essential role in oxygenating sediments and

645‐

controlling ecosystem services [121]. Furthermore, the energy assimilation of the

646‐

lugworm was compromised due to the suppressed feeding activity, and the faunal

647‐

diversity of the sediment habitats could be vulnerable. As the prey species for fish and

648‐

wading birds, the function of secondary producers may also be damaged during

649‐

ecosystem nutrient cycling [24]. As an emerging topic, the long-term or ecological

650‐

results have not yet been found, but such driving forces for the disturbance of

651‐

ecosystem productivity could result in alterations in biodiversity via defective

652‐

development of species, populations and communities.

653‐

5.2 Defective development of species, populations and communities

654‐

The detrimental impacts of microplastics on the growth and performance of

655‐

individual organisms threatens the development of the species and trophic-level

656‐

energy transfer, leading to nonfunctioning communities (Fig. 4.). The reduction in

657‐

biodiversity triggered by microplastics could also lead to defective community

658‐

development. The existence of microplastics at the nesting grounds in the northern

659‐

Gulf of Mexico altered the habitats of marine turtles (including the temperature and

660‐

permeability of the sediment), which negatively affected the incubation of this

661‐

endangered species [122]. Biodiversity contributes to the ecological flexibility of

662‐

ecosystems, and the interference in the lives and reproduction of endangered species

663‐

threatens their survival; further loss of biodiversity could disturb the normal

23‐ ‐

664‐

functioning of ecosystems [123]. Moreover, a negative impact on individual organisms or single species may be

665‐ 666‐

accumulated

and

magnified

an

disrupt

community

development.

Labeled

667‐

microplastics ingested by zooplankton were subsequently found in a mysid intestine,

668‐

which showed the transfer of microplastics from one trophic level (mesozooplankton)

669‐

to a higher level (macrozooplankton) [11]. Mytilus edulis mussels were exposed to

670‐

microplastics and experienced bioaccumulation and biomagnification; the mussels

671‐

were then fed to Carcinus maenas crabs, which also displayed bioaccumulation and

672‐

biomagnification [124]. Such trophic transfer could disturb the flow of energy in the

673‐

food web and the ecosystem. In addition, even without direct impacts on one specific

674‐

species, microplastics may still be detrimental for interspecies interactions (e.g.,

675‐

mutualistic relationship), which could cause a series of cascading effects in aquatic

676‐

ecosystems. For example, the damage to European flat oysters Ostrea edulis was

677‐

limited; the associated benthic accumulation structures, however, were altered by

678‐

microplastic exposure, and the species abundance and the total number of organisms

679‐

were decreased by ~1.2 and 1.5 times, respectively [125].

680‐

5.3 Microcosm interference

681‐

Microorganisms, which constitute more than 90% of the living biomass in the

682‐

ocean, dominate the abundance, diversity and metabolic activity in marine ecosystems.

683‐

Because microorganisms decompose marine organic matter, the variation in microbial

684‐

biomass and assemblages could change the carbon flux patterns and the

685‐

carbon-nitrogen cycle and modify the ecosystem function [126, 127]. Compared to

686‐

autochthonous substrates, the longer half-lives and hydrophobic surfaces of

687‐

microplastics promote strong affinities with microorganisms, which facilitates

688‐

microbial interaction, colonization and biofilm formation. After bacterial colonization

689‐

of this enduring habitat, plastisphere-specific bacterial assemblages with distinct

690‐

taxonomic compositions from the ambient environment develop rapidly [128, 129].

691‐

The colonization on microplastics alters the ecological function and the functioning of

692‐

microbial communities [130]. In a simulation of the elevated levels of nutrients and

24‐ ‐

693‐

the persistence of substrates, the functional diversity and biomass of the

694‐

microorganisms were affected due to changes in the heterotrophic activities on the

695‐

microplastics, which has potential impacts on global bacteria-driven ecosystem

696‐

processes such as C and N cycling [131]. Moreover, the transfer frequency of

697‐

plasmids carrying antibiotic resistance genes was found to be higher in the

698‐

microplastic-associated bacteria compared to the free-living bacteria, leading to

699‐

microcosm interference via evolutionary changes at the species and population levels

700‐

[132].

701‐

Another issue with the interference of microplastics with microcosms is that some

702‐

plastisphere members may be adaptable pathogens. The Arenicola atlantica gut

703‐

pathogens were detected on microplastics after the excretion; the ingestion of

704‐

microplastics by organisms is inevitable, and the bacterial assemblages would be

705‐

changed after passing through the digestive tract [133]. The occurrence of the human

706‐

pathogens Vibrio spp. on marine microplastics suggests that microplastics act as

707‐

vehicles for multitrophic level transfer of pathogenic microorganisms [134].

708‐

Aeromonas salmonicaida, one of the most harmful invasive bacteria responsible for

709‐

infections in the fish, was recently found on microplastics. The presence of A.

710‐

salmonicaida has rarely been recorded in the sea, but with the microplastics serving as

711‐

vectors, such pathogens may travel long distances and spread diseases on a global

712‐

scale [135].

713‐

5.4 Vulnerable specific aquatic ecosystem

714‐

The prevalence of microplastics in ecosystems with unique geographical

715‐

characteristics as well as indispensable functions (e.g., wetlands, estuaries, mangroves,

716‐

and deep ocean seafloor ecosystems) presents a higher risk of deteriorating the

717‐

vulnerable aquatic environments. Therefore, the microplastic disturbances in highly

718‐

sensitive ecosystems should be highlighted.

719‐

The intertidal zone, which connects terrestrial and aquatic ecosystems, is exposed

720‐

to a high risk of influence from microplastics due to its proximity to plastic debris

721‐

sources. Microplastic fibers were detected in the intertidal ecosystem of one exposed

25‐ ‐

722‐

beach and two protected beaches along the eastern shore of Nova Scotia [136]. The

723‐

highest microplastic concentration occurred at the high tide line on the exposed beach

724‐

because the low-density microplastic debris is more likely to be stranded at the upper

725‐

limits of the wave action in this high-energy environment. For the protected beaches,

726‐

the highest microplastic accumulation occurred in the low tide region due to the

727‐

enhanced deposition by the reduced waves and the altered properties of the

728‐

microplastics due to microbial films. The internal ecosystems were exposed to both

729‐

air and seawater and a high diversity of species were exposed to heightened risk to,

730‐

which may present unexpected impacts on both terrestrial and aquatic ecosystems

731‐

[136]. Prior to the transfer of water to the marine ecosystem, estuaries create

732‐

“brackish” waters by mixing the freshwater from river and saltwater from the ocean;

733‐

these areas have also been proven to be hotspots of microplastic contamination [137,

734‐

138]. The widespread microplastics in the estuaries and wetlands of southern Europe

735‐

and western Africa have been detected in sediment samples, macroinvertebrates, and

736‐

shorebird feces, indicating that the microplastics have entered into the food chain and

737‐

show evidence of transferring to the secondary intertidal consumers [139]. Another

738‐

valuable ecosystem located between the land and the ocean is the mangrove forest,

739‐

which transports nutrients from the land to estuaries and supports essential ecological

740‐

functions (e.g., intercepting land-driven nutrients, pollutants, and suspended matter

741‐

from travelling to deeper water; exporting materials for near-shore food webs; and

742‐

buffering against natural hazards) [140][141]. The prevalence of microplastics in this

743‐

ecosystem was identified in seven intertidal mangrove habitats in Singapore (up to

744‐

three times higher than the concentrations reported in the UK) due to the degradation

745‐

of marine plastic debris. The interference of microplastics may hinder mangrove

746‐

ecological system functions and reduce ecosystem services for coastal protection

747‐

[142].

748‐

Moreover, the invasion of microplastics into unknown regions is no longer the

749‐

most astonishing discovery. For instance, the deep sea is considered a major sink for

750‐

the microplastics [143]. Microplastics were first detected in pristine deep ocean

26‐ ‐

751‐

sediments worldwide in the polar front, Porcupine Abyssal Plain, distal lobe of Congo

752‐

Canyon, and Nile deep-sea Fan, indicating the spread of microplastics throughout the

753‐

unknown deep-sea regions [86]. After these findings, widespread microplastics

754‐

(42~6595 microplastic/kg) were detected in Arctic sea sediments at 2340~5570 m

755‐

depths. The accumulation and transport of microplastics may be attributed to sinking

756‐

algal aggregates and thermohaline circulation [81, 144].

757‐

Marine snow is another transport vehicle for microplastics into the abyssal depths

758‐

of the ocean. The sink rate for microplastics was shown to change significantly with

759‐

incorporation into the snow, changing from 818 m/day for the buoyant polymer

760‐

polyethylene to 916 m/day for the denser polyamide fragments, which increased the

761‐

bioavailability to benthic organisms [145]. After identifying microplastics in the deep

762‐

sea (>2200 m) at Rockall Trough, North Atlantic Ocean, the microplastics were

763‐

observed being ingested by benthic macroinvertebrates through various feeding

764‐

modes [146]. A True's beaked whale Mesoplodon mirus stranded on the coast of

765‐

Ireland was analyzed to study the ecology of the deep diving oceanic cetaceans, and

766‐

microplastics were found in the whale’s stomach [147]. As the largest yet least

767‐

studied ecosystem on earth, the ecological function and structure of the vulnerable

768‐

deep sea region may be altered by anthropogenic pressure [148, 149].

769‐

Likewise, for the Arctic aquatic ecosystem, microplastics were detected in

770‐

particularly high concentrations in the sea ice at Fram Strait, the Barents Sea slope,

771‐

and even in the remote Central Arctic [150]. Considering global climate change and

772‐

the yearly sea ice melt of between 1.6×104 km3 and 1.93×104 km3, the potential

773‐

release of microplastics was predicted at a minimum of 7.2×1020 and a maximum of

774‐

8.7×1020 particles/year between 2011 and 2016. The variation in the microplastic

775‐

pattern is prone to occur in areas with strong seasonal sea ice melt or outflow

776‐

gateways.

777‐

6. The contradictory opinions about microplastic toxicity & future research

778‐

perspectives The risk of microplastic toxicity has been the subject of a long-standing debate.

779‐

27‐ ‐

780‐

The main reasons that researchers have doubted the environmental risks of

781‐

microplastics are as follows:

782‐

1) The unrealistically high concentrations used during most experiments;

783‐

2) The incomparable sampling and analytical approaches used;

784‐

3) The failure to provide solid evidence for the toxicity effect and the

785‐

dosage-effect response in different studies.

786‐

For example, Kokalj et al. reported that facial cleanser microplastic particles were

787‐

not severely hazardous to isopods [151]. Hermsen et al. suggest that the toxicity of the

788‐

microplastics presented in the environment might be lower than anticipated due to the

789‐

asymmetrical approach conducted during the study [25]. Limited acute toxicity was

790‐

observed from the ingestion of microplastics by the Antarctic krill Euphausia superba,

791‐

and no mortality or the dose-dependent weight loss was observed; microplastics were

792‐

eliminated by most of the individuals without obvious bioaccumulation [152]. Rehse

793‐

et al. proposed that instead of accelerating, the microplastics reduced the short-term

794‐

effects of the environmental contaminant bisphenol A (BPA) and polycyclic aromatic

795‐

hydrocarbons by adsorbing and lowering the concentrations of the residual

796‐

contaminants to which the zooplankton Daphnia magna and microorganisms were

797‐

exposed [153, 154]. It was even pointed out that the penchant for visibility, the

798‐

pressure to publish, the inability to publish negative results, the need for funding, and

799‐

sensationalism might have stimulated the exaggeration of microplastics research

800‐

[155].

801‐

Nevertheless, studies that failed to provide visible acute toxicity evidence could

802‐

not discount the possibility of long-term chronic environmental disturbance when

803‐

considering the ubiquity and persistence of microplastics. As an emerging topic, the

804‐

different obscure microplastic-induced impacts could be easily overlooked. For

805‐

instance, one study found no evidence of increased mortality, impacted reproductive

806‐

parameters or morphological changes in the water flea Daphnia magna [156];

807‐

however, further observation revealed the alteration of gene expression as a stress

808‐

response. Additionally, nonlethal effects and reproductive interference were observed

28‐ ‐

809‐

in Hydra attenuata, and disruption of feeding behaviors and changes to morphology

810‐

were observed that were certainly caused by microplastics [99]. On the one hand, the

811‐

transfer of PCBs from microplastics under simulated gut fluid conditions is fully

812‐

biphasic and reversible, even decreasing the bioavailability of the chemicals present in

813‐

the gut [157]. On the other hand, the ingestion of microplastics enhances the PAH

814‐

biomagnification due to the reduction in the fraction of PAHs available for

815‐

metabolization [158]. Organisms have been shown to respond to microplastic toxicity

816‐

in minor and diverse ways, and the complexity of the actual environment and the

817‐

insufficient consideration by unsound studies could lead to ambitious conclusions.

818‐

With decades of work, more research has started to conduct experiments with

819‐

environmentally relevant parameters [159], and attempts have also been made to

820‐

determine the true environmentally relevant toxicity by analyzing the microplastic

821‐

debris from the susceptible organisms stranded on beaches [147]. The potential

822‐

impacts of microplastics on organisms and the environment had been revealed

823‐

gradually, and the possibility for transfer among different trophic levels and food

824‐

webs has been studied and confirmed [11, 124]. Without a better understanding of the

825‐

ecological consequences triggered by microplastics, it may not be urgent to push the

826‐

government to implement harsh bans on the use of microbeads; however, intense

827‐

management of microplastic contamination should be encouraged.

828‐

For now, the interference of microplastics may appear to be an unimpressive

829‐

“minor disease” for the aquatic ecosystem: irritating, yet with unclear and

830‐

nondestructive consequences. The insufficient attention paid may eventually make

831‐

this issue more serious; when the occurrence of severe consequences appears to be

832‐

solid, we will owe the future generation an explanation for why we neglected this

833‐

problem. Several reviews have discussed and explained that microplastics present no

834‐

risk to the aquatic environment (Adam et al. 2018, Besseling et al. 2018, Burns et al.

835‐

2018), and the attention from different perspective during this debate should be

836‐

regarded as an opportunity to broaden the collective knowledge and should encourage

837‐

researchers to further advance the toxicological studies of microplastics. Therefore,

29‐ ‐

838‐

we further emphasize the significance of studying microplastic contamination of

839‐

different biota in various environmental settings. Researchers should consider

840‐

focusing not only on the identification of the effects on the specific species but also on

841‐

the broader ecological implications of the effects of microplastics. Based on decades

842‐

of microplastic toxicological studies and the shortcomings discussed, the following

843‐

perspectives are suggested for future research:

844‐

1) Instead of presenting the common physiological parameters of microplastics

845‐

and the response of organisms generally, the comprehensive consideration of

846‐

the potential impacts should be considered based on the features of the

847‐

microplastics and the behavioral and biological characteristics of organisms.

848‐

2) Multiple species of organisms and types of microplastics should be used for

849‐

toxicological risk assessments, and not only the acute toxicity but also the

850‐

sublethal chronic endpoints and the ecotoxicological investigations at

851‐

different trophic levels should be considered further.

852‐

3) A database of the microplastic toxicity for different biota should be developed

853‐

systematically, and the adaptability of the existing toxicological analysis

854‐

models for microplastics should be tested. 4) The joint toxicity with environmental contaminants and the long-term

855‐

ecological consequences should be further investigated.

856‐ 857‐

5) Standardized methodology for the analysis of microplastic contamination and

858‐

toxicology should be regulated, and a parallel comparison with different

859‐

research should be conducted to advance the understanding of the general

860‐

toxicity pattern of microplastics.

861‐

The present review not only presented an overview introduction for all

862‐

researchers investigating of the potential impacts of microplastics but also provided a

863‐

framework for researchers to complete their work more systematically.

864‐ 865‐

Acknowledgments

866‐

This work was supported by the National Natural Science Foundation of China

867‐

(No. 41772264) and the Research Fund of State Key Laboratory of Geohazard 30‐ ‐

868‐

Prevention and Geoenvironment Protection (SKLGP2018Z001)

31‐ ‐

Table 1. The translocation of microplastic within different species (a. Biological response reported in the research; b. Potential impact proposed in the literature)

Species

Translocation spot

Biological response & Potential impact

Ref.

Bivalve mussel Mytilus edulis (L.)

circulatory system, Restricting blood flow causing damage to the vascular tissues and [35] hemolymph changes in cardiac activity b

Invertebrate Daphnia Magna

lipid storage droplets

Fiddler crab Uca rapas

Reducing ecosystem service (e.g., processing of organic matter) gills, stomach, due to the low performance of organisms, leading to far-reaching [161] hepatopancreas consequences for the coastal habitats b

Decreasing energy reserves for metabolism and growth; Transfer [160] from mother to newly created egg b

Hemolymph, tissues Bioaccumulation and biomagnification during the trophic transfer Mussel Mytilus edulis (L.) Shore crab Carcinus Stomach, gills, and between mussel and crab, leading to vulnerable larval and juvenile [124] Maenas stages of the crab a ovary Gilt-head seabream Sparus Aurata

Liver, muscles

Causing inflammation, lipid accumulation, oxidative stress at [162] higher exposure concentration b

Zebrafish larvae

The heart region

Triggering systemic immune responses

European anchovies Engraulis encrasicolus, L

Hepatic Tissue

Leaching chemicals (adsorbed pollutants and additives) into the [163] blood and other organs; enhanced vascular thrombosis b

Barnacle larvae Amphibalanus Amphitrite

Bloodstreams to Included in metamorphosis and settled into the juvenile form, tissue and other parts persisting in other parts of the body and tissues throughout stages [164]. of the body of growth and development a

Blue Mussel Mytilus edulis L.,

Adopted into cells of Causing significant effects on the tissue and cellular levels, [165]. the digestive system histological changes, and inflammatory response a

32‐ ‐

[22]

Table 2. The combined effects of the inorganic and organic pollutants adsorbed on the surface of the microplastic

Inorganic

Microplastic

Pollutant

Species

Toxic effect

The acute toxicity test showed PS Abnormalities, including Polystyrene/Polyst exhibited a slight antagonistic effect on Ni Daphnia Magna immobilization and changes in yrene-COOH Ni toxicity, whereas PS-COOH had a morphology. synergistic effect with Ni. Accumulated the metal in the brain and muscles, causing European Fluorescence red neurotoxicity, oxidative stress Preadsorption for Hg on the seabass polymer Hg and damage, and changes in the microplastic accumulated the Dicentrarchus microspheres activities of energy-related accumulation of Hg in tissues. labrax enzymes in juveniles of this species. MPs and natural organic matter aggravated the accumulation and zebrafish Danio Accumulation in tissue and toxicity of Cu. The levels of Polystyrene Cu rerio toxicity to guts and liver. malonaldehyde and metallothionein were increased, and the superoxide dismutase was decreased. Accumulated Ag between the rainbow trout four intestinal compartments of No disturbance effect on the Polyethylene Ag Oncorhynchus the mucus layer, mucosal accumulation mykiss epithelium, muscle layer, and serosa. Polychlorinat Lugworm Bioaccumulation and influence Microplastic contributed marginally to Polyethylene ed biphenyls Arenicola feeding activity bioaccumulation. (PCBs) marina (L.) 33‐

‐

Combination Effect

Ref.

[62]

[166]

[167]

[168]

[169]

Polyvinyl chloride

Organic

Polyethylene microbeads (MP)

Chiral antidepressan t venlafaxine and its metabolite O-desmethyl venlafaxine (pharmaceuti cals) Triclosan (TCS) hydrophobic organic contaminants (HOC)

polyethylene (PE), polystyrene (PS), Triclosan polyvinyl chloride (TCS) (PVC), and PVC800 Procainamid Red fluorescent e and polymer doxycycline microspheres (pharmaceuti cals) Fluorescent POPs microplastic polycyclic

Loach Misgurnus anguillicaudatu s

Microplastic facilitated the transfer and Accumulating in loach tissues bioaccumulation of contaminants to the [170] and liver subcellular. liver and postpone the contaminants metabolism in organisms

Marine copepod Acartia tonsa Bioaccumulation metabolic Microplastic potentiates TCS-mediated [171] (Dana) activity and mortality. toxicity due to the adsorption capacity.

Microalgae Skeletonema costatum

Toxicity of microplastics on microalgae mainly resulted from physical damage, and the triclosan showed inhibition effect on the growth of microalgae.

marine microalga Tetraselmis chuii

Toxicological interaction with Reduced growth rate and the microplastic increased the adverse [173] chlorophyll concentration. toxic effect.

Artemia nauplii Desorb in the intestine and Functioned as a vector to facilitate the [174] and transferred to the intestinal contaminant transfer at different 34‐

‐

Th Joint toxicity of TCS and microplastic was all antagonism, and the antagonistic effects increased with [172] the higher adsorption capacity of triclosan

particles

aromatic hydrocarbon benzo[a]pyre ne (BaP)

zebrafish

epithelium and liver

Bioaccumulation of phenanthrene-derived residues in Polystyrene plastic 14C-phenanth Daphnia Magna daphnia body and inhibited the particles rene dissipation and transformation of phenanthrene in the medium. Accumulation in hemolymph, gills and especially digestive Polycyclic mussel tissues. alterations of Polyethylene (PE) Aromatic Mytilus immunological responses, Polystyrene (PS) Hydrocarbon galloprovinciali lysosomal compartment, s (PAHs) s peroxisomal proliferation, antioxidant system, neurotoxic effects, the onset of genotoxicity Japanese PAHs/PCBs/ Polyethylene (PE) medaka Oryzias PBDEs latipes Polyethylene (PE) Virgin industrial microplastic Benzo[a]pyre Polypropylene Fish cell line extract has no toxic effect on fish ne (PP) cell line

35‐ ‐

trophic levels

The adsorption capacity enhances the [175] toxicity

Adsorption elevate bioavailability and [176] toxicological pathway of the chemicals

Altered the functioning of the [112] endocrine system in aquatic animal Benzo[a]pyrene coated extracts increase EROD activity and DNA damage

Fig. 1. The microplastics resembling the prey were more likely to be ingested (blue microplastic debris ingested due to the confusion with the blue copepods [34]) (Obtained copyright permission, Science of The Total Environment, Elsevier, 4543940873342, Mar 07, 2019)

36‐ ‐

Fig. 2. The molecular structures of the most common microplastics and the interactions with environmental contaminants

37‐ ‐

Fig. 3. a. The microplastics translocated within the zebrafish larvae away from the injection site [22] (obtained copyright permission, Aquatic Toxicology, Elsevier, 4543950272607, Mar 07, 2019); b. accumulation of polystyrene microbeads in the gills, liver, and gut of Eriocheir sinensis [177] (obtained copyright permission, Aquatic Toxicology, Elsevier, 4543950630725, Mar 07, 2019).

38‐ ‐

Fig. 4. The overall framework for the toxicological mechanism and the ecological implication: the microplastic enters the marine food chain and transfers throughout the different trophic levels; the environmental pollutants adsorb on the microplastics or the plastic additives and are released after ingestion; the widespread microplastics affect the individuals, then the population, before finally disturbing the community structure and function.

39‐ ‐

Fig. 5. The result microplastic toxicity on ecology

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50‐ ‐

Highlights


MPs properties determined bioavalibility and toxicity
Spatical and temporal dynamic affect MPs ingestion by organism
A series of damage and physiological response caused by MPs ingestion
MPs disturbance showed potential of triggering ecological consequences

Microplastics in Aquatic Environments: Toxicity to Trigger Ecological Consequences

Ma Hui 1, 2, Pu Shengyan1, 3, 4,*, Liu Shibin1, Bai Yingchen3, Sandip Mandal1, Xing Baoshan4 1

State Key Laboratory of Geohazard Prevention and Geoenvironment Protection (Chengdu University of Technology), Chengdu 610059, Sichuan, China;

2

Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 401871 Frederiksberg, Denmark

3

State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China

4

Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA 01003, United States

The authors declare that there is no conflict of interests regarding the publication of this paper.

*

Corresponding author at: State Key Laboratory of Geohazard Prevention and Geoenvironment Protection (Chengdu University of Technology), Chengdu 610059, PR China. Tel./fax: +86 (0) 28 8407 3253; E-mail: [email protected]; [email protected] (S.Y. Pu); [email protected](B. Xing) Notes: The authors declare that there is no conflict of interests regarding the publication of this paper.