Authors: Huirong Yang, Yinglin He, Yumeng Yan, Muhammad Junaid, Jun Wang
Categories: Review, atmosphere, characteristics, distribution, microplastics, quantitative analysis, toxicity
Source: Nanomaterials
Doi: 10.3390/nano11102747
Microplastics (MPs) (including nanoplastics (NPs)) are pieces of plastic smaller than 5 mm in size. They are produced by the crushing and decomposition of large waste plastics and widely distributed in all kinds of ecological environments and even in organisms, so they have been paid much attention by the public and scientific community. Previously, several studies have reviewed the sources, occurrence, distribution, and toxicity of MPs in water and soil. By comparison, the review of atmospheric MPs is inadequate. In particular, there are still significant gaps in the quantitative analysis of MPs and the mechanisms associated with the toxic effects of inhaled MPs. Thus, this review summarizes and analyzes the distribution, source, and fate of atmospheric MPs and related influencing factors. The potential toxic effects of atmospheric MPs on animals and humans are also reviewed in depth. In addition, the common sampling and analysis methods used in existing studies are introduced. The aim of this paper is to put forward some feasible suggestions on the research direction of atmospheric MPs in the future.
Keywords: microplastics, atmosphere, distribution, characteristics, toxicity, quantitative analysis
A significant number of previous studies have emphasized the ubiquitous presence of microplastics (MPs) in the oceans [1], freshwater bodies [2,3], and soil [4], along with food items, drinks [5], seasonings [6], and aquatic organisms (Figure 1). Microplastic pollution in the environment can be caused by several factors, including landfills [7]; dumping and application of sewage sludge [8]; fiber shedding of synthetic textiles; transportation (wear of tires, brakes, road signs, etc.) [9]; and other human activities, including industrial plastic pellet preproduction [10], plastic mulching and grinding in agricultural [11], fisheries, and tourism [12]. After being released into the environment through different pathways, these microplastics experience the process of degradation (physicochemical fragmentation, chemical aging, biological degradation, etc.) [11] and translocation [13] under different environmental conditions. Finally, they enter animals and humans through skin contact, oral ingestion, inhalation, and other ways and continue to get enriched [14]. After entering the body, microplastics may produce a variety of negative effects, such as decreased growth rate [15], inflammatory response [16] and oxidative stress [17], and metabolic disorders [18]. In severe cases, they can penetrate organs [19,20], tissues [21], and even cells [22], causing toxic effects. Because microplastics have a large specific surface area and strong adsorption capacity, they easily adsorb various inorganic pollutants, such as Cu, Pb, and Cd, [23] and organic pollutants, e.g., PCBs [24], PAHs [18], and polybrominated diphenyl ethers [25]. Even some microplastics themselves contain additives with a certain toxicity, and some studies have shown that microplastics combined with these pollutants pose a serious threat to organisms.
Figure 1 Cycle of microplastic pollution in ecosystems.
MPs in the air have been identified as particulate air pollutants and paid great attention recently [26]. However, at present, the research on environmental MPs is mainly focused on the aquatic ecosystem, and the number of studies on atmospheric MPs is limited, which is a limitation to further understanding the environmental characteristics and negative effects of atmospheric MPs. The small size of MPs, especially nanoplastics (NPs), facilitates their emissions into the air [27] and long-distance transportation [28] and can cause adverse effects on animals and humans through respiratory inhalation [29]. Critical analysis is urgently needed to open new ways of thinking about atmospheric MPs in the future.
In this review, the research progress on atmospheric MPs in recent years is summarized, including the (1) the global distribution of atmospheric MPs and their influencing factors, (2) the origin and fate of atmospheric MPs, (3) advances in sampling and analysis of atmospheric MPs, (4) toxicological impacts of MPs in the atmosphere on animals and humans, and last but not the least (5) the existing gaps in each part and the corresponding future research directions.
At present, the relevant studies on the distribution of MPs mainly pay attention to the water and soil environment and the number of studies about atmospheric MPs is limited (Table 1). The earliest research on the distribution of atmospheric MPs can be traced back to Dris et al. collected and analyzed samples of outdoor air in Paris’s urban areas, where the concentration of MPs ranged between 29 and 280 items/m^2^/day. The size of MPs ranged from 0.1 to 5 mm, and the shapes mainly included fibers and fragments [30]. In another study, Dris et al. measured that the number of MPs in indoor air in Paris reached 5.4 items/m^3^, while that in outdoor air in the same area was only 0.9 item/m^3^, indicating indoor human activities among the major sources of MPs in indoor settings [31].
Subsequently, studies on atmospheric MPs have been carried out around the world, including a dozen countries and regions in Asia [33,34,38,39,47], Europe [36,43,45], and the Arctic [48]. The survey areas include urban sites, such as municipal areas [38], apartments [31], offices [31], industrial areas [40], terminals [35], and universities [47], as well as suburbs [32], rural areas [27], mountains [42], straits [46], estuaries [46], oceans [41,46], glaciers [28], and even the planetary boundary layer (PBL) [27]. These studies suggest that MPs exist in the atmosphere worldwide, from near the ground level up to 1.5 km high.
Similar to other air particle pollutants, the concentration of atmospheric MPs near the ground is much higher than that at high altitudes due to the influence of gravity [49]. Li et al. also demonstrated this phenomenon by collecting atmospheric plastic particle deposition on the ground and on the roof of buildings in the urban areas of Beijing, where the concentration of particles in the former was higher than that in the latter [47]. However, this does not mean that MPs in the atmosphere are not worth taking seriously. Gonzalez-Pleiter et al. found MPs in the atmospheric particulate matter samples collected by the spacecraft in the planetary boundary layer (PBL) [27]. These studies suggest that MPs are ubiquitous in atmospheric environments, ranging from near the ground to high altitudes.
Dris et al. found that rainfall affects the sedimentation rate of microplastic fibers in the atmosphere of Paris. When rainfall is 0–0.2 mm/day, 2–34 items/day are recorded. When the rainfall reaches 2–5 mm/day, the amount of sediment increases to 11–355 items/day [32]. This indicates that rainfall has a significant effect on the precipitation behavior of atmospheric MPs. Boucher et al. pointed out that 7% of atmospheric MPs are transported into the ocean by wind [50], indicating that low-density atmospheric plastic particles can pollute other ecosystems through the wind as a medium. However, Prata et al. believe that atmospheric microplastic particles have properties similar to other particulate pollutants and meteorological factors such as wind, precipitation, and temperature will have an impact on their concentration changes [49]. These studies indicate that meteorological conditions are a significant factor influencing the distribution characteristics of atmospheric MPs.
Numerous studies have shown that the concentration of MPs in the indoor air environment is much higher than that in the outdoor within the same area. Dris et al. conducted a study on the outskirts of Paris in 2015, where they analyzed microplastic fibers in the air outside and inside apartments and found that these man-made fibers are mostly polypropylene (PP). Moreover, the fiber concentration in indoor air (0.3–1.5 (0.9) items/m^3^) was significantly higher than that in outdoor air (0.4–59.4 (5.4) items/m^3^) [31]. When the outdoor environment is crowded enough, the concentration of MPs in the atmosphere can reach very high levels. Kaya et al. analyzed the concentrations of atmospheric MPs in universities and terminals with a large population in Sakarya Province, Turkey, in 2016–2017, and found concentrations of particles as high as 10,495–30,822 particles/L [35]. The high concentration of airborne MPs in indoor and crowded outdoor environments may be attributed to similar conditions of high population density and poor particle dispersion capacity.
Varying distribution of atmospheric MPs was observed in different regions. The concentrations and types of atmospheric MPs in different urban areas have similarities and differences. Cai et al. analyzed the concentration of MPs (175–313 items/m^2^/day) in the urban air of Dongguan in 2016 and found that the content of fibers in the air was the highest (90.1%), followed by fragments (6.8%), film (2.9%), and foam (0.2%)) [33]. In the same year, Zhou et al. carried out a similar investigation in the urban area of Yantai and found that the concentration of atmospheric MPs was 130–640 particles/m^2^/day, with a higher occurrence of fiber (95.05%), followed by fragments (4.04%), film (0.73%), and foam (0.18%) [34]. The concentration of atmospheric MPs varies in different regions, which may be influenced by local meteorological conditions, the topography, the urban heat island effect, and other factors [51]. However, the types of atmospheric MPs in different regions and urban areas show high similarity. Fibers are observed as the absolute dominant shape for atmospheric MPs, while fragment, film, and foam MPs appear in significantly low quantities. It is known that microplastic fibers mainly come from synthetic textiles. Fragments may come from disposable plastic bags, film may be obtained by breaking thick plastic products, and foam may come from foamed plastics [33]. It is suggested that the atmospheric MPs in central urban areas mainly come from the shedding of synthetic textiles.
Atmospheric MP concentrations often differ between urban and suburban areas. Dris et al. collected and analyzed the deposition from the air in the urban and suburban areas of Paris during 2014–2015, and the concentration of MPs in the former (110 ± 96/m^2^/day) was much higher than that in the latter (53 ± 38/m^2^/day) [32]. The higher intensity of human activity in urban areas may have contributed to higher concentrations of atmospheric MPs. The similarity of occurrence between the two (mainly fiber) may be due to atmospheric migration that leads to regional homogenization.
However, it appears that not all suburban and remote areas have a low atmospheric microplastic distribution. Allen et al. collected atmospheric sediments from the Pyrenees Mountains in France in 2017–2018 and reported an MP concentration of 365 ± 69 items/m^2^/day. It was dominated by polystyrene and polyethylene. The occurrence was fragments (68.0%), film (20.0%), and fiber (12.0%) [42]. Ambrosini et al. collected and analyzed atmospheric sediment samples from the Forni Glacier in the Alps in 2018, and the concentration of MPs in the samples was 74.4 ± 28.3 items/kg of sediment. MP polymer types included polyester (39%), polyethylene (9%), polyamide (9%), and polypropylene (4%). Fibers accounted for 65.2%, and fragments accounted for 34.8% [52]. It can be seen that remote areas may also have high concentrations of atmospheric MPs and there are great differences in the concentrations and types among different regions.
At present, due to large differences, it is still difficult to draw a clear picture of the regional distribution of atmospheric MPs, to identify the most polluted areas, so it is necessary to master more methods to study atmospheric MPs.
From the above-reviewed studies, we found that the current research on the distribution of atmospheric MPs is relatively limited and there is a lack of clear and systematic studies. To this end, we propose the following for future
Synthetic textiles are a major source of atmospheric MPs. The output of synthetic textiles in the world has been growing gradually year by year. Since the annual output exceeded 60 million tons in 2016, it has been growing steadily by about 6%/year [53]. The commonly used plastic raw materials in synthetic textiles include fiber with polymers of polyamide (PA), polypropylene (PP), polyacrylonitrile (PAN), polyester (PET), polyvinyl formaldehyde (PVDF), polytetrafluoroethylene (PTFE), etc. In the use of synthetic textiles, fine fibers fall off from the fabric and are released into the air due to grinding and cutting in the textile industry, as well as wearing, washing, and drying clothes in daily life. It has been reported that thousands of fibers can be shed from a single gram of PAN fabric [54]. According to a study of De Falco et al., there is a significant correlation between the shedding of microplastic fibers (MFS) during the wearing of synthetic clothing and the type of fabric. Taking PES as an example, short silk fabrics release more MFS than filament fabrics, which may be because short fibers are easier to shed during movement, friction, and other behaviors. However, knitted garments are more likely to shed MFS than woven garments, which may be due to the looser arrangement of fabric fibers in knitted garments [55]. COVID-19 is wreaking havoc around the world, leading to a global surge in the production and use of masks and protective clothing. Mask and protective clothing materials are known to include PP, polyethylene (PE), polyurethane (PU), PTFE, PET, and ethylene side-by-side (ES) polymer plastics [56]. These anti-epidemic fabrics may become a major source of atmospheric MPs in coming years. In addition, because the inside of a mask is close to your mouth and nose, the MPs they shed can be easily inhaled.
Transportation also contributes a lot to atmospheric MPs, for example, in the form of wear particles from the tires and brakes of cars as well as from road surfaces and aircraft tires [9,57]. Existing research suggests that the composition of tire and road wear particles (TRWPs) is about 50% natural or synthetic polymers, which include a large number of plastic components, such as styrene–butadiene rubber (SBR). It shows that a great number of plastic particles enter the surroundings each year because of TRWP emission [58], accompanied by a certain amount of preservatives, antioxidants, desiccants, plasticizers, and other additives. According to Wagner et al., road traffic alone produces 1.327 million tons of TRWPs per year in Europe. These TRWPs can easily pollute the air environment through direct discharge or resuspension of road dust [59]. The world produces 0.2–5.5 kg of TRWPs per person per year, of which the contribution to PM10 emissions accounts for 11%. Moreover, TRWPs make up more than 50% of MP emissions in Denmark and Norway, as well as about 30% in Germany [60]. In addition, TRWPs are usually emitted in heterogeneous aggregates with other wear particles present in traffic (brake wear, road wear, etc.) [61].
The concentration of MPs in ambient dust is very high, both in deposited dust and in suspended dust. In terms of deposited MP particles, the distribution of MPs of different shapes and sizes is very uneven under the influence of external forces (natural or human activities), and they are easily suspended in the atmospheric environment due to external forces. However, the form of MPs in floating dust is mainly fine fibers. Compared with other types of plastics, the lower-density characteristics of MPs facilitate their suspension in air [40]. Liu et al. studied and analyzed indoor and outdoor dust samples from 39 cities in China and found that PET majorly contributes to the content of MPs in indoor dust. This may be because indoor MPs are mainly derived from synthetic fabrics and PET is the main component of polyester in commonly used synthetic fabrics, which are easy to use, wash, and dry. Secondly, polycarbonate (PC), which is widely used in electronic equipment, hardware, and food packaging, can also easily fall off and enter the atmosphere [62,63].
Atmospheric MPs are also likely to come from the degradation of large plastics, such as building materials and synthetic furniture; landfills; synthetic particles from gardening; and industrial and other emissions-related activities. However, compared with the major sources of MPs such as synthetic textiles, transportation, and dust, the actual contribution of these sources to atmospheric MPs may be very small and remains in the stage of idea and speculation, without the availability of data [32,33,38].
From the above series of articles, it is found that the current articles on the sources of atmospheric MPs are mostly focused on synthetic textiles, transportation, dust deposition, and resuscitation, while other sources are often ignored, and the contribution of these sources to atmospheric MPs cannot be quantified. Detailed data on their pollution concentrations, types, and occurrence are scarce. In the analysis of the sources of atmospheric MPs in many pieces of literature, the proportion of unknown sources in the experimental results is relatively high, indicating that there is still a considerable part of atmospheric MP sources that is unclear. In addition, many research methods to identify the origin remain in the characterization and chemical composition analysis. To this end, we propose the following for future
Under certain conditions, MPs in the air can migrate to other ecological environments (soil, water, etc.). Their behavior, transportation, concentration, and deposition are affected by various factors, such as vertical pollution concentration gradient (VPCG) [64,65], meteorological conditions (rainfall, precipitation, temperature, humidity, wind (occurrence, velocity, duration, intensity, and direction), etc.) [39,42,43,66], population density, human activities [32,39], urban topography, thermal cycling [51,64], local elevation, and geographical environment [39]. Some researchers have found that MPs travel long distances in the air. For example, MPs are found in extremely remote areas and even in the snow and ice of high-altitude glaciers. It is speculated that MPs cause cross-border and global pollution through air and wind currents [27,28].
Since the MP concentration indoors is much higher than that outdoors, atmospheric MPs enter the body through human inhalation [31]. Indoor air is an essential source of human exposure to airborne MPs because people stay indoors for longer periods and dispersing machines are less capable of removing plastic particles [49]. Factors affecting MP behavior and transmission in indoor air are ventilation, airflow, and room spacing [67]. The concentration of MP particles indoors is higher than that outdoors, which may be influenced by textiles, furniture, building materials, and human activities [31]. Compared with MPs in other environments, MPs indoors are more easily inhaled directly and continuously and cause health risks [49,53].
One of the earliest criteria for determining airborne MPs is 0.3–1.5 particle/m^3^ outdoors and 0.4–56.5 particles per cubic meter indoors (33% polymer) [31]. According to statistics, each person inhales between 26 and 130 MP particles from the air per day [49]. Based upon air samples taken from mannequins, men who exercise lightly can expect to inhale 272 particles/day [44]. Estimates vary depending on sampling methods and space use factors.
Based on the above discussion, the studies on the fate of MPs in the atmosphere are limited. So far, only limited studies have traced the atmospheric migration paths of MPs; therefore, it is nearly impossible to quantify the various environmental factors and human activities affecting the behavior and transmission of atmospheric MPs. Further, the quantification and characterization of atmospheric MPs in different parts of the human body and associated health impacts is challenging. To this end, we propose the following for future
After the body inhales MPs, they enter the lungs along the trachea, enter the blood vessels through migration, and then spread through the circulatory system throughout the body, causing various degrees of toxic effects on the cells, tissues, organs, and systems of the body (Figure 2) [19,68,69,70].
Figure 2 Toxic effects of atmospheric microplastics on different organs and systems.
MPs and NPs in the air mainly enter animals and humans through inhalation and first contact with the respiratory system. Due to the clearance mechanisms of the respiratory barriers (such as the nasal cavity, trachea, the bronchus, and alveolar macrophages), a considerable proportion of these plastic particles cannot enter the body and form deposition, and the deposition coefficient is mainly affected by the particle size, density, etc. [49]. Smaller nanoparticles (<2.5 μm) can avoid the clearance mechanism and penetrate the lung and respiratory barrier [19,68,69,70]. Macrophages can deposit plastic particles in the respiratory system, remove these from the respiratory system, or help them migrate in the respiratory system and allow them to enter the circulatory system, leading to dust metastasis. Further, the presence of MPs and NPs in the respiratory system and their large surface area can also lead to the release of chemokines that affect the migration of macrophages, resulting in particle overload [68]. The influx and inflammation of neutrophils associated with polystyrene granules (64 nm) in rat lungs, as well as the expression of pro-inflammatory genes in epithelial cells, are caused by granule-induced oxidation [71]. Due to the large specific surface area of MPs, a large number of oxidizing substances (such as metals) will be adsorbed on the surface of MPs, which may produce excessive reactive oxygen species and lead to excessive antioxidant reaction in vivo, namely oxidative stress [72,73].
There are only a few pieces of research on the toxic effects of atmospheric MPs on animals and humans. Inhalation of MPs has the most significant toxic effects on the respiratory system. Studies have shown that PVC prepared by emulsion polymerization (2 mm) has significant cytotoxic and hemolytic effects on rat and human lung cells in vitro [74]. Xu et al. 2002 [74] evaluated the toxic effects of PS-NPs on human alveolar epithelial cells and found that PS-NPs can rapidly internalize into cells; significantly reduce cell viability; affect cell cycle and apoptosis, as well as related gene transcription and protein expression; and promote inflammatory response. The smaller the diameter, the faster the corresponding velocity. Lim et al., using metabonomics to investigate the toxic effects of PS-NPs on bronchial epithelial cells, found that nanoparticles interfere with cell energy metabolism, accompanied by oxidative stress, and mediate the increase of intermediate metabolites to reduce cell resistance to toxicity [75]. Dong et al. found that PS-MPs can induce cytotoxicity and inflammation in human lung epithelium by inducing reactive oxygen species formation. Low concentrations of PS-MPs disrupt the lung barrier, while high concentrations of PS-MPs also induce decreased levels of α 1-antitrypsin, which increases the risk of chronic obstructive pulmonary disease [76]. Paget et al. explored particle internalization and cell damage after aminated PS-NPs acted on human lung epithelial cells and macrophages. Cells in the experimental group showed high glutathione depletion, excessive reactive oxygen species, and significant DNA damage. It is suggested that micro- and nanoplastics may exhibit strong genotoxicity when absorbed and internalized by the respiratory system [77]. In in vitro experiments, seven functional groups with different charges were added to an aminated PS-NPs and eight PS-NPs, including the original particles, were sent into different rats by pharyngeal aspiration. Most of the particles were phagocytized by alveolar macrophages and showed different acute lung inflammation. The particle potential showed excellent correlation with pneumonia-related parameters, indicating that surface charge is a key factor affecting lung inflammation induced by micro- and nanoplastics [78].
Respiratory lesions have been found in workers exposed to synthetic textiles, fusing, vinyl chloride, or PVC, which is quite different from the general population [79,80,81,82,83]. Inhaled MPs and NPs are not easily cleared by the human lungs, and they may stay in the lungs for a considerable period, which can cause an inflammatory response in the lungs [53]. It is reported that artificial glass fiber can cause DNA damage, which can induce cancer [84]. In short, Inhaling MPs can have toxic effects on animals and humans.
The inhaled MPs can also have negative effects on other systems of the body, such as diffusion or translocation. In vivo experiments have confirmed that microplastic particles can enter the circulatory system through the migration of macrophages after inhalation [68]. MPs in the circulation system may cause inflammation, vascular occlusion [85], and other blood toxicity [86]. In vitro experiments showed that polystyrene nanoparticles cause red blood cell (RBC) aggregation, while polypropylene particles increase hemolysis [87]. Inhaled MPs may enter the gastrointestinal tract by clearing upper respiratory tract cilia [53]. MPs entering the digestive system may alter the permeability of intestinal epithelial cells and cause changes in microbial composition [88]. Recent reports have found that after maternal lung exposure to NPs, the plastics can enter the placenta and the fetus through translocation and get deposited in the fetal liver, kidney, nervous system, and circulatory system. [21]. There is little research on the toxic effects of atmospheric MPs on systems other than the respiratory system, and more research must be done to explore their effects on animals and humans.
MPs usually contain various additives, e.g., catalysts (organotin), flame retardants, polybrominated diphenyl ethers [89], antioxidants (nonylphenol), antibacterial agents (triclosan), and plasticizers (phthalate PAEs) [90]). All of them are harmful to animals and humans. In addition, MPs adsorb many inorganic pollutants in the environment, e.g., Au [16] and Cu [91], and organic pollutants, e.g., polycyclic aromatic hydrocarbons [18] and polychlorinated biphenyls [92]. These pollutants are mutagenic and carcinogenic substances that are widely present in the environment. In addition, many plastic monomers themselves (polystyrene (PS), polyvinyl chloride (PVC), etc.) have mutagenic and carcinogenic toxic effects on animals and humans [93]. Exposure of animals and humans to additives or adsorbents in these plastic particles results in combined toxicity (Table 2). MPs in the atmosphere are most likely to combine with other pollutants in atmospheric environments (such as POPs and Cu) and serve as carriers for the long-distance transport of these pollutants in the atmosphere [53]. Some articles have studied the negative effects of MPs combined with these pollutants on animals and the human body, such as a series of oxidative stress [16], inflammatory reaction [91], and metabolic disorders [18]. There is a risk of mutation and carcinogenesis [94]. Most of these studies have involved oral ingestion or in vitro studies. However, there are few studies on the toxicity mechanism of these binding substances after they enter animals and humans through inhalation, and more experimental data are needed.
In conclusion, studies on the quantitative analysis and toxicity mechanism of atmospheric MPs inhaled by animals or humans are scarce and these aspects need to be further studied. To this end, we propose the following for future
There are two main sampling methods for atmospheric MPs commonly used. One way is to collect the passive fallout from the atmosphere and filter it. The depositions in the atmosphere are collected through a non-plastic funnel (such as stainless steel or glass) the pipe of which drops into a glass collection bottle below. MPs can then be easily filtered out of the sediment [32,33,42,43]. Another method is active pump sampling and filtration, mainly through a set of pumping and filtration system, in which air is collected through the pump unit and then filtered through the filter to retain the plastic particles [31,38,40]. After the sample is collected, different efficient quantitative analysis methods can be used to analyze the types and sizes of particles (Table 3).
Although a set of primary collection and analysis methods has been established, there are still many limitations and deficiencies. The above methods can only identify some common types of plastic particles at the ground level or near the ground level [27]. Moreover, it is difficult to accurately identify the size of the nanoplastics or the types of particles adsorbed by organic matter on their surfaces [101,103,104]. To this end, we propose the following for future
MPs have been well studied in marine and freshwater environments, but MPs in the atmosphere have received little attention from researchers and society. Microplastics in the atmosphere enter the body mainly through inhalation and further systemic exposure, causing toxic reactions and disorders in various organs and systems and even posing a potential risk of cancer to animals and humans.
Due to the lack of practical methods for detection and analysis, we are still unable to gain a more detailed understanding of the global distribution, sources, and fate of atmospheric MPs, let alone further elucidate the mechanisms of toxic action of atmospheric MPs on animals and humans. We suggest that the scientific community conduct in-depth research on atmospheric MPs in the future, especially to explore relevant sampling and detection methods and establish a common industry standard. Further quantitative analysis of atmospheric MPs of different types and properties will be conducted to explore the toxicity mechanism and additive effect of their combination with other pollutants through in vivo experiments.
Conceptualization, H.Y. and J.W.; methodology, Y.Y.; software, Y.H.; validation, H.Y. and J.W.; formal analysis, Y.H. and Y.Y.; investigation, M.J.; resources, H.Y. and Y.H.; writing—original draft preparation, H.Y. and Y.H.; writing—review and editing, H.Y. and Y.H.; visualization, Y.H.; supervision, H.Y. and J.W.; project administration, H.Y. and J.W.; funding acquisition, H.Y. and J.W. All authors have read and agreed to the published version of the manuscript.
This study was funded by the National Key Research and Development Program of China (2018YFD0900604), the Guangdong Forestry Science and Technology Innovation Project (2021KJCX012), Provincial Science and Technology Special Fund Project for Zhongshan City (major special project + Task list management mode) (2021), Rural Science and Technology Commissioner Service Team project of New Rural Development Institute, South China Agricultural University (2021XNYNYKJHZGJ022), Provincial Projects with Special Funds for Promoting Economic Development of Marine and Fisheries Department of Guangdong (SDYY-2018-05), the Project of Guangzhou Association for Science & Technology (K20200102008), the Guangdong Province Universities and Colleges Pearl River Scholar Funded Scheme (2018), the National Natural Science Foundation of China (42077364), the Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) (311021006), and Key Research Projects of Universities in Guangdong Province (2019KZDXM003 and 2020KZDZX1040). We appreciate the provision of SCAU Wushan Campus Teaching & Research Base.
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The authors declare no competing financial interests.
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