Impact of size and shape in the transport of microplastics by a springtail species

ABSTRACT

We investigated the impact of shape (beads, fibers and films) and size (0.5 and 1.0 mm; diameter or length) of polypropylene microplastics (MPs) on MP transport by a springtail species, Folsomia candida in dishes. The percentages of transported beads, fibers and films were 9.10%, 3.18% and 4.10%, respectively. For 1.0 mm MPs, the number of MPs transported was significantly higher for beads than for fibers and films, whereas, for 0.5 mm MPs, the number was significantly higher for fibers than for the other MP types. Additionally, the number of MPs transported was higher for small fibers than for large fibers, whereas it was higher for large beads than for small beads. These results indicate that the effects of F. candida on MP migration depend on MP shape and size. Our results highlight the importance of considering the physical characteristics of MPs while elucidating the interaction between soil fauna and MPs.

KEYWORDS:

• Folsomia candida
• microarthropods
• microplastics
• springtail
• transport

1. Introduction

Microplastics (MPs) are plastic particles <5 mm in size and are increasingly recognized as an important environmental problem in aquatic and terrestrial ecosystems [1,2]. Microplastics enter the soil via mulch degradation, car tire wear, domestic laundry and plastic landfills [3–6]. The limited recovery and inefficient degradation of plastics lead to the accumulation of MPs in soil. MP pollution in soil ecosystems can threaten human safety and soil organisms [7]. However, the majority of research on this topic has focused on aquatic ecosystems [8–10]; as a result, our understanding of MP pollution in soil ecosystems is limited.

Exploring the migratory mechanism of MPs in soil ecosystems is crucial for predicting the associated ecological and environmental risks. MPs that enter the soil environment are transported by various abiotic [11–15] and biotic factors [16–18]. Soil fauna is an abundant group of organisms including earthworms, springtails and mites [19]. These organisms can substantially contribute to the maintenance and function of soil ecosystems by mediating key ecosystem processes, such as litter decomposition and nutrient mineralization [19–21]. They are thought to facilitate the transport of MPs in the soil. Previous studies have explored the roles of various soil fauna, including earthworms [22–24], mites [25], springtails [25,26] and ants [27] in the horizontal and vertical transport of MPs. For example, earthworms can transport MPs during ingestion, digestion and excretion [22–24], and springtails and mites can move MPs via surface attachment, grasping and pushing [25,26]. Given the abundant soil fauna in soil ecosystems and their roles in MP transportation, soil fauna-induced MP transport may pose a potential threat to other organisms and the whole soil ecosystem (including groundwater) [23].

MPs commonly occur in the environment as either primary or secondary MPs [28]. Primary MPs are produced purposely for use in personal care products, whereas, secondary MPs are degraded products of larger plastic waste [29]. Owing to their manufacturing origin and environmental degradation, MPs may occur in many shapes and sizes [30–33], and these different physical characteristics may have different effects on soil properties [34,35] and invertebrates [36]. For example, smaller-sized MPs are easier to ingest [37] and are supposedly more toxic to soil fauna [38,39], whereas fibers are supposedly more toxic to invertebrates than beads (under specific experimental conditions) [40]. Despite these results, previous studies have mainly explored the ecotoxicological effects of MP characteristics on organisms, and little is known about the effects on transport (review in [41]). Moreover, although several existing studies have assessed the effects of MP size on soil fauna-mediated MP transport [23,26,42], the interaction of MP size and shape on this process remains unclear.

This study aimed to explore the effects of MP shapes and sizes on its transport by soil fauna. Among soil fauna, the springtails constitute an important component of soil fauna, and their activities have a significant impact on ecosystem functions such as organic matter decomposition [43]. The springtail Folsomia candida (Collembola) was chosen for this study as they are considered to be transport agents for MPs [25,26]. Polypropylene (PP) plastic type was selected as the MP model in various shapes (including beads, fibers and films) and size to replicate the large amounts of PP that have persisted and accumulated in the soil [44]. We hypothesized that (1) the number of transported beads would be higher than that of transported films and fibers because spherical objects roll more readily than non-spherical objects; and (2) the number of small MPs transported would be higher than that of the large MPs because of their lighter mass.

2. Materials and methods

2.1 MPs and soil fauna

In this study, PPs of three different shapes (beads, fiber and films) and two sizes (1.0 and 0.5 mm; diameter or length) were used. All the materials were purchased online (Ruixiang Polymer Material Business Department, Guangdong Province, China). The film PPs were manually cut with micro-scissors into squares with edge lengths of 1.0 or 0.5 mm. The fiber PPs were cut into lengths of 1.0 or 0.5 mm. The bead PPs with diameters of 1.0 or 0.5 mm was selected using a vernier caliper. These PPs were washed with ethanol (70%) and deionized water to remove the solvent chemicals on the surfaces.

Springtails are abundant in soil ecosystems and play an important role in the food webs [45]. A common springtail species, Folsomia candida, was selected in this study because of its wide distribution, short generation time and parthenogenetic reproduction [42]. F. candida is commonly used as a standard species to investigate the ecotoxicological effects of MPs [17] and the transport mechanism of MPs [25,26]. In the present study, the F. candida individuals were purchased online. Before the experiment, F. candida individuals were reared in laboratory and fed on dried baker’s yeast twice a week. F. candida individuals with the same age and body length (approximately 3 mm) were used in this study.

2.2 Experimental design and setup

The experiment was performed in plastic Petri dishes (9 cm diameter). Four concentric circles 3 (zone 0), 5 (zone 1), 7 (zone 2) and 9 cm (zone 3) in diameter were drawn around the center of each dish (Figure S1). Then, 500 MPs were evenly distributed in zone 0 of each dish. Six treatments (three shapes × two sizes) were set up, and 25 F. candida individuals were placed in zone 3. Each treatment was assigned seven replicate dishes for each treatment and a control dish that did not contain F. candida for each of the treatment, resulting in a total of 48 dishes (three shapes × two sizes × seven replicates + six controls). We covered the inside of the lids of each dish with moist tissue to maintain the moisture content, and the lid was used to prevent airflow. The dishes were then incubated at 20 ± 2°C. No additional food source was provided. Each dish was photographed every day for 7 days, and the number of MPs in each zone was recorded. The transport percentage of MPs in each dish was calculated as the number of removed MPs × 100%/500.

2.3 Statistical analysis

Generalized linear mixed models (GLMMs) were used to examine the fixed effects of MP shape, size, zone, and their interactions on the number of MPs removed. The replicates were included as random effects. If significant effects were detected, post-hoc least significant difference tests (LSD) were used to evaluate the significance of differences. P < 0.05 was considered statically significant.

3. Results

3.1 The transport of PP MPs by F. candida

F. candida behavior facilitated the transport of MPs from zone 0 to other zones (Figure S2). The F. candida touched the MPs with their legs or heads when they crawled over them, leading to MP transport. Additionally, we observed that the attachment of fibers to the body and legs of F. candida occasionally led to MP transport. The percentages of beads, fibers and films transported by F. candida were 9.10%, 3.18% and 4.10%, respectively. After 7 days, most transported MPs were observed in zone 1, and the number of transported MPs was substantially greater in zone 1 than in zones 2 and 3. No MPs were detected in zone 1, 2 or 3 of the control dishes.

3.2 Effects of MP shape, size, zone and their interactions on the MP transport

Overall, the number of transported beads was significantly higher than that of the transported fibers and films (Table 1; Figure 1(a)). The MP shape and its interaction with MP size and/or zone significantly influenced the number of MPs transported (Table 1; Figure 1(c); Figure 2). For the 1.0 mm MPs, the number of transported beads was significantly higher than that of transported fibers and films in zone 1 (Figure 2; F = 12.36, P < 0.001) but no significant differences were found in zone 2 (Figure 2; F = 0.912, P = 0.42) or zone 3 (Figure 2; F = 0.27, P = 0.76). For the 0.5 mm MPs, the number of transported fibers was significantly greater than that of transported beads and films in zones 2 (Figure 2; F = 4.91, P = 0.02) and 3 (Figure 2; F = 12.21, P < 0.001). However, no significant differences were found in zone 1 (Figure 2; F = 2.69, P = 0.10).

Figure 1. Mean number (mean ± SE) of MPs transported by F. candida. Different letters above the bars indicate significant differences between the shapes (a), sizes (b) and sizes with the same shapes (c).

Figure 2. Mean number (mean ± SE) of beads, fibers and films transported by F. candida in zone 1, zone 2 and zone 3. Different letters above the bars indicate significant differences among shapes in each zone (capital and lowercase letters for 1.0 mm and 0.5 mm MPs, respectively). The asterisk (*) indicates significant differences between sizes in each zone.

Table 1. Results of GLMMs of the effects of microplastic (MP) size, shape and zone on the MP transported by Folsomia candida. Significant results are in bold.

	df	F	P
MP shape	2	11.821	0.001
MP size	1	5.295	0.061
Zone	2	100.753	<0.001
MP shape × MP size	2	4.791	0.03
MP shape × zone	4	17.311	<0.001
MP size × zone	2	7.496	0.008
MP shape × MP size × zone	4	2.707	0.054

MP size did not influence the number of MPs transported (Table 1; Figure 1(b)). However, the size-shape-zone interaction significantly influenced the number of MPs transported (Table 1; Figure 1(c); Figure 2). For beads, the number of transported 1.0 mm MPs was significantly higher than that of transported 0.5 mm MPs in zone 1 (F = 6.73, P = 0.02). For fibers, the number of transported 0.5 mm MPs was significantly higher than that of the transported 1.0 mm MPs in zone 3 (F = 15.19, P < 0.01). However, no significant differences were observed in the other treatments (Figure 2).

4. Discussion

In soil ecosystem, the transport and dispersion of MPs are important processes. MPs in soil undergo vertical and horizontal migration under abiotic and biotic conditions [14,17,23]. Although previous studies have reported that soil fauna such as springtails plays an important role in this process [25,26,42], the effects of size/shape-different MPs on this process remain unexplored. Our results clearly show that the combination of MP shape and size considerably affects the transport of MPs by F. candida.

The shape of MPs is considered an important factor that influences their migratory behaviors in the environment [46–48]. Some studies have investigated the effects of abiotic factors such as runoff [15] and dry-wet cycles [49] on the MP migration and found that the migration capacity depended on MP shape. However, to the best of our knowledge, the effects of MP shape on soil fauna-mediated MP migration have been largely neglected. In the present study, the results revealed a significant difference of migration among three shape-different MPs. The number of MPs transported was higher for beads than for fibers and films (Figure 1). In theory, spherical objects roll more readily than non-spherical objects. This difference may partly explain the highest migration capacity of beads, as well as the similar migration capacity between fibers and films. Moreover, bead MPs have a relatively small surface area compared to film or fiber MPs [15]. This difference may lead to the higher horizontal mobility of bead MPs than film or fiber MPs in soil under simulative rainfall [15]. Future research should attempt to assess the impact of surface area of MPs on the soil fauna-induced MP migration. Although further investigations are needed, our results suggest that soil fauna-induced MP migration is shape-dependent.

In addition to MP shape, MP size can also affect the MP migratory process [50,51]. Therefore, in the present study, F. candida was expected to transport more of the smaller MPs than the larger ones. Contrary to our hypothesis, MP size did not significantly affect the number of MPs transported by F. candida (Figure 1). This is in line with the study by Maaβ et al. [26], which showed that MP size had no significant effect on the number of urea-formaldehyde MPs transported by two Collembolan species. Why MP size had no effect on the number of MPs transported by F. candida remains unclear. A possible explanation for this phenomenon is that the ability to transport is limited in F. candida due to its small body size. The results of this study and previous work studies found that only a very small proportion of the added MP particles were moved by F. candida [25,42]. The limited transportation ability of F. candida may lead to a similar transport pattern for size-different MPs. For larger soil fauna, such as earthworms, Rillig et al. [23] found that smaller polyethylene (PE) microbeads were transported downward by earthworms to a greater extent than were the larger ones. It seems that the effect of MP size on MP transport is associated with soil fauna identity, particularly body size. Moreover, the experiment duration (1 week) in this study might not sufficient to examine the effects of MP size. Indeed, Luo et al. [42] recently found that the F. candida exhibited a greater ability to transport small PP MPs than large ones within 4 weeks. Therefore, studies of long-term experiments are necessary to assess the effects of MP size on soil fauna-induced MP transport.

Although MP size did not affect the number of transported MPs, its interaction with MP shape did. For example, although small fibers were more prone to transport in general, large beads were more prone to transport in zones 1 and 2 (Figure 2). This difference may be attributed to the transport mechanism. Previous studies have reported that F. candida can move MPs by surface attachment, grasping and pushing [25,26]. In this study, we found that F. candida accidentally move the fiber MPs by surface attachment, whereas they usually move the beads by grasping and pushing. Further research is needed to determine if these distinct behaviors could cause interaction effects. Overall, this indicated that the specific combination of MP size and shape can influence the fauna-mediated MP transport. As MPs have diverse characteristics, such as size, shape, color, chemical composition and chemical additives [52,53], further studies are necessary to explore the interactive effects of various MP characteristics on MP transport by soil fauna.

5. Conclusions

In this study, we confirmed that F. candida transported MPs within a laboratory setting. We have also found that the MP shape-size interaction affected the transport processes by F. candida. Exploring the factors affecting MP migration in soil ecosystems is crucial for predicting the ecological risks posed by MPs. Our findings provide important information for the management and disposal of MPs in soil ecosystems. Although we have investigated the impact of MP shape and size on MP transport by F. candida, the potential ecotoxicological impact of size/shape-different MPs on F. candida was not explored. In addition, MPs in soil can be ingested by springtails, which may affect the springtail behavior and migratory process of MPs [17,42]. An important next step will be to assess the effects of size/shape-different MPs on soil fauna behavior and the ingestion-induced MP migration.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/26395940.2023.2261776

Additional information

Funding

The work was supported by the Natural Science Foundation of Jiangsu Province (BK20210631), the National Natural Science Foundation of China (42101106) and the Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX23_1127).