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Article

Virgin and Photoaged Polyethylene Microplastics Have Different Effects on Collembola and Enchytraeids

by
Elise Quigley
1,*,
Ana L. Patrício Silva
2,
Sónia Chelinho
3,
Maria J. I. Briones
1 and
Jose P. Sousa
4
1
Departamento de Ecología y Biología Animal, Universidad de Vigo, 36310 Vigo, Spain
2
Centre for Environmental and Marine Studies (CESAM) & Department of Biology, University of Aveiro, 3810-193 Aveiro, Portugal
3
Polytechnic Institute of Coimbra, 3045-093 Coimbra, Portugal
4
Centre for Functional Ecology, Associate Laboratory TERRA, Department of Life Sciences, University of Coimbra, 3000-456 Coimbra, Portugal
*
Author to whom correspondence should be addressed.
Environments 2025, 12(6), 175; https://doi.org/10.3390/environments12060175
Submission received: 18 April 2025 / Revised: 20 May 2025 / Accepted: 21 May 2025 / Published: 25 May 2025
(This article belongs to the Special Issue Ecotoxicity of Microplastics)
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Abstract

:
Wariness is increasing about resident times of microplastics (MPs) in soils; however, limited knowledge is available on ultraviolet (UV) light exposure of MPs to soil fauna. This study investigated the effects of virgin and photoaged polyethylene microplastics (PE MPs) on soil mesofauna (enchytraeids and collembolans) at environmentally relevant concentrations in a microcosm incubation experiment. Ten individuals of each Enchytraeus crypticus and Folsomia candida and twenty Proisotoma minuta were exposed separately to virgin and photoaged PE MPs (40–48 μm) admixed in agricultural soil (0.2–2000 mg/kg) to evaluate reproduction and survival. After 28 d of exposure to photoaged PE MPs, there was a moderate survival reduction but reproduction promotion of E. crypticus. Contrastingly, F. candida exhibited an opposite trend, with survival enhancement and reproduction depression rates when exposed to both PE MP contaminated soils. However, P. minuta was the only species with significant apical endpoint changes after PE MP exposure; at 20 mg/kg photoaged and 2000 mg/kg virgin PE MP exposure, there was a 34% and 31% decrease in survival, respectively, and at 200 mg/kg photoaged PE MP exposure, an increase of 39% for reproduction. PE MPs had contrasting impacts on soil mesofauna species, which highlights the need to account for these variable results when understanding the repercussions of MP pollution on community assemblage and population dynamics in soils.

1. Introduction

Plastic contamination has materialized into a problem, extending past the scope of just aquatic compartments. As of 2015, 79% (~6300 Mt) of all generated plastic litter since 1950 is in nature or landfills [1]. Terrestrial environments are major recipients of this considerable amount of plastic debris, from macro- to micro- and nanoplastic size fractions [2]. Considering small-sized fractions such as microplastics (MPs), terrestrial environments can present 4–23 times greater concentrations in relation to aquatic habitats [3]. Average concentrations of MPs in conventional agricultural soil have been estimated to be 4.5 mg/kg [4], whereas highly contaminated soils situated near industrial sites can range up to 67,500 mg/kg [5].
The resident times of MPs in any system invariably subject them to weathering and aging [6]. Ultraviolet (UV) radiation is one of the major contributors to microplastic weathering [7,8]. The changing properties under UV irradiation (e.g., surface roughness, morphology, and chemistry) of aged MPs result in different effects on the soil environment, chemical interactions, and organisms [9]. UV irradiated polystyrene (PS) MPs have caused neurotoxicity and reproductive inhibition in the nematode Caenorhabditis elegans [10], and the earthworm Eisenia fetida experienced myriad toxicological impacts when exposed to H2O2 aged polyethylene microplastics (PE MPs) in soil, from tissue damage to gut dysbiosis and more [11]. Still, little has been researched regarding aged MP effects on soil fauna [10,12,13,14,15]. So far, most studies carried out with soil fauna addressed the ecotoxicity of virgin MPs, and several adverse effects were observed at considerably higher concentrations than the ones reported in the field, such as increased mortality, decreased reproduction, gut microbiome dysbiosis, intestinal injury, oxidative stress, and neurotoxicity, among others, in nematodes, enchytraeids, collembolans, woodlice, and snails [16].
The aim of this study was to investigate the effects of environmentally realistic concentrations of virgin and photoaged PE MPs on the survival and reproduction of three mesofauna species: Enchytraeus crypticus (Oligochaeta: Enchytraeidae), Folsomia candida (Collembola: Isotomidae) Willem, 1902 and Proisotoma minuta Tullberg, 1971 (Collembola: Isotomidae). Enchytraeids and collembolans represent two dominant groups of mesofauna in the top 5–10 cm soil layer (biomass >104 individuals/m2 [17]) that are crucial in organic matter (OM) breakdown and nutrient mobilization as well as bacterial and fungal colony control [18,19,20,21]. The active breakdown of surface OM by these two groups may contribute to MP comminution and incorporation into the soil [22,23,24], which would suggest direct interaction and possible ingestion of MP particles. With the wide range of soil ecosystem functions that these species provide, it is essential to evaluate potential hazards to their health and survival.
Polyethylene (PE) was chosen as the test polymer due to its high abundance in agricultural soils [25], mostly related to intensive application of PE-based agricultural mulching film [26]. Removal of plastic PE-based mulching film is <60%, leading to large quantities of plastic being subjected to UV photodegradation and weathering, effectively fragmenting and accumulating PE MPs in cultivated soils [3,6]. Additionally, PE is the second most abundant plastic found in sewage sludge, next to PS [27], which is globally used as agricultural soil fertilizer [28]. In this study, we employed a wide range of concentrations of both virgin and photoaged PE MPs with environmental relevance [4,5]. Many of the studies formerly mentioned above that found MP impacts on soil species do not reflect environmentally relevant concentrations, yet the marked changes that can occur to plastic once it enters an ecosystem are highly variable and depend on many factors that ultimately result in vastly different outcomes [29,30]. Therefore, we hypothesize that inhibition of survival and reproduction might be exacerbated with increasing concentration levels of PE MPs in soil. Additionally, we expect photoaged PE MPs to induce more profound effects than virgin PE MP exposures.

2. Materials and Methods

2.1. Microplastics

Polyethylene (PE) particles (40–48 μm size average; ultra-high molecular weight powder, CAS No. 9002-88-4, density 0.94 g/mL at 25 °C) were acquired from Sigma-Aldrich, Gillingham, UK. Particle sizes of PE MPs were selected based on previous studies that tested ingestion capabilities of the species used in this experiment [24,31]. Two PE MP treatments were prepared for exposure tests, i.e., virgin and ultraviolet irradiated (photoaged). PE MPs were subjected to ultraviolet light for 24 h per day for 16 days to obtain photoaged PE MPs. PE MPs were irradiated under a UV-C lamp (VL-6.LC Vilber, Germany; 254 nm wavelength, 6 Watt per light tube), throughout which monitoring of the PE MPs was carried out twice daily with three recordings for intensity maintenance with a lux meter wand (Delta Ohm HD 9221). After aging procedure, Attenuated Total Reflectance-Fourier transform infrared spectroscopy (ATR-FTIR) (Thermo Scientific Nicolet 6700; Thermo Nicolet Corp., Madison, WI, USA) was utilized to measure surface chemical changes on PE MPs (n = 3). ATR-FTIR equipment was connected to a diamond crystal ATR accessory (Smart Orbit) (CACTI, University of Vigo, Vigo, Spain). Spectra of the PE MPs sample were measured at an angle of incidence of 45° (one reflection) in the range of 400 to 4000 cm−1 with a resolution of 4 cm−1 while using a KBr beamsplitter and a deuterated triglycine sulfate (DTGS) detector. Each PE MP sample was scanned 32 times, then analyzed using the OMNIC program. The carbonyl index of the spectra was estimated using the area under 1650–1800 cm−1 over the area under 1420–1500 cm−1 (Almond et al. [32]; adjusted equation), representing the carbonyl band (C=O) and methylene band (CH2), respectively.
Silva et al. [33] gauged PE MP particle size distribution. In brief, a vibrating sieve shaker sieved PE MP (100 g) using mesh aperture sizes: 32, 63, 125, 250, and 500 μm. A total of 94.36 ± 1.36% of our particles fell in the range of 63–32 μm, and 5.54 ± 0.96% were <32 μm.
Before and after use, the equipment was sterilized using ethanol (96%) after washing with acid or soap and water. Airborne plastic contamination was minimized by covering samples and filters, and by using only glass equipment. Cotton lab coats were used routinely to prevent microplastic contamination of synthetic fiber origin.

2.2. Experimental Soil

An organic agricultural plot (Herdade do Freixo do Meio, 440 ha, 38°42′13.2″ N, 8°19′31.4″ W) supplied the test soil from southern Portugal (Montemor-o-Novo, in the region of Alentejo). In the field, sieving was performed (5 mm). Before exposure, the soil was defaunated by freezing, and then it was thawed. Information on soil physicochemistry and texture was conducted by the Laboratório de Análise de Solos e Plantas at the Universidade de Trás-os-Montes e Alto Douro and is provided in Table S1. The soil was classified as sandy loam with an organic matter (OM) content of 3.0 ± 1.02% (average ± SD) and a pH (KCl) of 4.93 ± 0.12. Water holding capacity (WHC) was recorded at 47.03 ± 0.91% (average ± SD).

2.3. Model Organisms

Two Collembola species Folsomia candida (Collembola: Isotomidae) Willem, 1902 and Proisotoma minuta Tullberg, 1971 (Collembola: Isotomidae), and one enchytraeid species, Enchytraeus crypticus (Oligochaeta: Enchytraeidae) were obtained from stock cultures (Universidade de Coimbra, Portugal). Collembolans were housed in plastic containers containing substrate of activated carbon with Plaster of Paris (1:11, w:w), saturated with distilled water. Distilled water was added weekly while aerating the plates and granulated dry yeast was fed ad libitum. Collembolans were frequently transferred into fresh containers, by tapping or using a manual exhauster, to induce oviposition. Active adults (~200 individuals) were transferred to a fresh substrate for egg laying (around 2 d) to obtain F. candida and P. minuta individuals with synchronized ages, the adults were subsequently removed. Newly hatched juveniles were removed from the remaining eggs to new substrates for culture. Enchytraeus crypticus [34,35] were housed in culture soil in the lab in plastic vessels with perforated lids and fed ad libitum with rolled oats. Cultures maintained a light:dark cycle of 16 h:8 h at 40–50% humidity and 20 ± 2 °C in the culture lab. Approximately one week before the start of the exposure periods ~300 adults were selected under a stereomicroscope to ensure clitellum was developed, then moved to new agar plates.

2.4. MP Exposure

For all three mesofauna species, concentrations of 0, 0.2, 2, 20, 200, and 2000 mg PE MP/kg of soil dw were mixed in soil for virgin and photoaged PE MP treatments, no more than one week prior to exposure start date and kept refrigerated in the meantime. These concentrations correspond with 0.00002, 0.0002, 0.002, 0.02, and 0.2% of dw soil and are considered to be environmentally realistic densities found from terrestrial sampling [4,36]. PE MP particles, at different concentrations, were admixed in soil with distilled water for 5 min to meet 40% of soil water holding capacity (WHC). Experimental soils were moved to jars (50 mL), each containing 20–30 g of soil. Treatments and controls had five replicates each, with one replicate jar, having no organisms added, being used to measure soil pH (KCl) and water content before and after the test period (n = 4).
Controls were prepared with no addition of PE (virgin nor photoaged), one control for each start date of exposure. For E. crypticus and P. minuta, the virgin and photoaged soil incubations started on separate days; hence, there were two control treatments for each of these species. F. candida’s virgin and photoaged soil exposures fell on the same date, so we used one control for this species. Exposures followed ISO 16387 [34] guidelines for E. crypticus and ISO 11267 [37] for collembolan species. Ten clitellate E. crypticus adults were randomly added to their respective test jars; 30 jars in total. The enchytraeids were fed 10 mg of rolled oats once a week. Ten F. candida and twenty P. minuta, both aged 10–12 days, were distributed to their respective treatments and given 5 mg of granulated dry yeast weekly. Twenty P. minuta individuals were used due to the fact that they are a sexually reproducing species with lower rates of multiplication. To maintain 40% of WHC, water was added each week through mass loss to every replicate.
After 28 days of exposure, the replicates were dismantled. E. crypticus individuals were fixed by adding 96% ethanol generously above the soil level in every jar of each replicate containing organisms, additionally 5 mL of Bengal rose (Sigma Aldrich; 1% in ethyl alcohol) was added to E. crypticus jars to dye their bodies. After 48 h of dyeing E. crypticus individuals, the soils were washed through a 0.25 mm mesh, and then adults and juveniles were counted under a stereomicroscope. F. candida’s soil was transferred into plastic bowls, flooded with distilled water, stirred for a minute to release all organisms from soil matrix and allow floatation and dyed with dark blue ink. Plates were then staged and imaged, then images were processed using ImageJ (Version 1.53) to facilitate counting of adults and juveniles. P. minuta were extracted from each replicate into 96% ethanol filled falcon tubes (50mL) using a Macfadyen extractor at 45 °C for at least 48 h and then dyed with 5 mL of Bengal rose for at least an additional 48 h and counted under a stereomicroscope to record numbers of surviving juveniles and adults.

2.5. Statistical Analyses

Levene’s test was used to test homogeneity of variances and Shapiro–Wilk test for normality. Based on homoscedasticity and normality of data distribution, the following parametric tests were performed. A two-way ANOVA was used to analyze survival and reproduction using PE MP concentration level and type (virgin and photoaged) as variables, followed up with a post hoc LSD test. One-way ANOVAs were used to compare concentrations among individual PE MP type, followed up with a post hoc LSD test. Due to non-normal FTIR data, Mann–Whitney U tests were performed to compare the individual FTIR spectra peaks created by virgin and photoaged PE MPs. GraphPad Prism 9 was utilized to perform all tests. Data are presented as average ± standard deviation.

3. Results

3.1. Chemical Changes from Virgin to Photoaged PE MPs

Virgin and photoaged particles’ FTIR spectra present comparable peak distribution, with slight changes in their intensity (Figure 1). Carbonyl index did increase from virgin to photoaged PE MPs, 0.032 to 0.038, respectively; however, the increase was not significant. This increase would indicate that some degradation is occurring. In photoaged PE MPs, there were significant decline in the characteristic peaks of methylene functional groups at 2915 cm−1 (p < 0.05) and 2848 cm−1 (p < 0.05). Peak widening also occurred at 3300–3500 cm−1 and 1712 cm−1.

3.2. Effects of Virgin and Photoaged PE MPs on Mesofauna Survival and Reproduction

There were no significant changes in soil pH or water content between treatments or over the duration of the test (28 d). Initial and final averages of these values are reported in Table 1. Validity of tests were met, according to ISO 16387 [34] guidelines for E. crypticus and ISO 11267 [37] for collembolan species; mortality in the controls were below 20% for all species, the number of juveniles was above 25 for enchytraeids and above 100 for both collembolan species. Finally, reproduction’s coefficient of variation was no more than 50% for enchytraeids and 30% for either collembolan species.
E. crypticus, P. minuta, and F. candida survival is presented in Figure 2 and reproduction is presented in Figure 3.
There was no effect of PE MP (virgin and photoaged) concentrations on E. crypticus survival (F (5,47) = 1.258; p > 0.05) (Figure 2A) or reproduction (F (5,47) = 0.6109; p > 0.05) (Figure 3A). However, there was a decrease in survival in almost all the PE MP exposures. There were greater increases in reproduction when incubated with photoaged compared to virgin PE MP, rising up to 20 mg/kg photoaged PE MP with an increase of 12.63 ± 18.58%, while there was a decrease in survival at every photoaged PE MP concentration. No trend like this was found among virgin PE MP exposures, where reproduction tended to remain similar among concentrations.
There was no effect of PE MP concentrations on F. candida survival (F (5,48) = 0.9288; p > 0.05) (Figure 2B) or reproduction (F (5,48) = 0.905; p > 0.05) (Figure 3B). When incubated with photoaged PE MP the survival was greater than virgin PE MP exposure. F. candida reproduction was not significantly different overall between virgin and photoaged PE MP (F (1,48) = 0.8326; p > 0.05), yet reproduction of this collembolan species decreased in almost all treatments and concentrations, with the greatest reduction of 26.83 ± 22.3% at 200 mg/kg virgin PE MP.
P. minuta survival was affected when exposed to virgin (F (5,19) = 2.44; p < 0.05) as well as photoaged (F (5,23) = 0.494; p < 0.05) PE MP concentrations, with a general decrease in adult numbers (Figure 2C). Survival was significantly decreased by 30.93 ± 6.23% at the highest concentration (2000 mg/kg) of virgin PE MP (p < 0.05), and even more so decreased by 34.1 ± 8.55% at a moderate concentration (20 mg/kg) of photoaged PE MP (p < 0.05). Likewise, there was an interaction between PE MP aging and level of exposure for adult survival (F (5,42) = 2.548; p < 0.05).
Reproduction among P. minuta was not impacted by increasing concentrations of either PE MP type (F (5,42) = 0.604; p > 0.05). Yet there were higher numbers of juveniles at almost every concentration of both PE MP types (Figure 3C); however, compared to virgin, the increase in reproduction was significantly more pronounced when incubated with photoaged PE MP (F (5,42) = 11.47; p < 0.05). The highest increase in reproduction was 39.47 ± 10.66% (p < 0.05) when exposed to 200 mg/kg photoaged PE, this was also heightened significantly in relation to that of virgin reproduction at the same concentration (p < 0.05). There is an interesting trend among P. minuta, where survival generally decreases, while reproduction generally increases with PE MP exposures.

4. Discussion

There has been a growing body of research regarding terrestrial microplastics in the last decade; however, every material classified as an MP is not equally comparable given their vastly different chemical composition, physicochemical properties, concentration, and distribution in a given media. For the experimental MPs in this present study, we selected the most prevalent MP recovered from agricultural soils, polyethylene [25], with >48 μm in size at environmentally relevant concentrations of 0.2–2000 mg/kg in soil, in their virgin and photoaged form. Through exposures we found decreased survival and increased reproduction trends emerged significantly for P. minuta and insignificantly for E. crypticus when incubated with photoaged PE MP, whereas F. candida conversely had unchanged survival and insignificant decreases in reproduction when incubated with both virgin and photoaged PE MP.
In their virgin form, our results suggest that PE MPs exert no major alterations in terms of survival and reproduction on both collembolans and enchytraeids. We only have evidence, among virgin PE MP exposures, of a significant decrease of 31% in the survival of P. minuta at the highest concentration (2000 mg/kg). Pristine polyethylene MPs have been seen to affect collembola survival at much larger concentrations, like decreases in F. candida survival up to 28% at 10 000 mg/kg of PE MPs (<50–500 μm) [38]. Yet, the effects of virgin PE MPs on soil organisms are highly variable for apical endpoints when considering similar concentrations, mostly depending on the tested concentration and particle size. For example, on one hand, collembolan species, F. candida, reproduction decreased when exposed to PE MP concentrations > 1000 mg/kg when considering particle sizes of <50–500 μm [38], while mobility was inhibited in soil at the same concentration of PE MPs but when particle size was around 20–30 μm for Lobella sokamensis [39]. A similar reproductive reduction in virgin PE MP exposure was seen only for one of our species in the present study, F. candida (decrease of up to 27%); however, it was nonsignificant. This reduction in F. candida reproduction is also supported by previous exposures to other MP particles, where PVC (80–250 μm) exposure at 1000 mg/kg decreased reproduction by 28.8%. Th authors here presumed that collembola chose MPs as a primary site for egg deposition, potentially impacting the abundance, dispersal, and viability of the eggs [40]. Conversely, there has been more evidence of polyethylene MPs exerting no significant impact on like species at concentrations and sizes similar to ours. Enchytraeid’s survival and reproduction were not affected when exposed to 320–6400 mg/kg PE MP with an average size of 68 μm [41]. Similarly, nematodes exposed to HDPE fragments (<250 μm) in soil did not affect the number of offspring at 1000 mg/kg [42]. Furthermore, woodlice exposed to PE MPs saw no change in mortality or immune markers at 200, 600, and 1700 mg/kg (39.5 μm) [43]. It seems that the range of lower, environmentally relevant concentrations in these size ranges of PE MPs do not impact population or apical endpoints (survival, reproduction, growth, etc.) very much. Likewise, in the present study, we did not see a good case for impacts of virgin PE MP particles overall on the apical endpoints of reproduction or survival among our mesofauna species.
Aging and degradation of MPs can substantially change the particles chemically and physically, but it can also change the way it interacts with other particles and with environmental matrices and invertebrates. Chemical degradation through UV irradiation is usually the initial and most profound degradation process for plastics including chain scission, creation of functional groups containing oxygen, and cross-linking [44,45]. The UV aging process increased the carbonyl index of PE MP in this present study, yet not significantly. There were, however, significant decreases in the characteristic peaks of methylene functional groups at 2915 cm−1 and 2848 cm−1, the change in intensity at these bands are sufficient to assume early stages of chemical modifications in degradation [46]. This was along with the formation of hydroxyl/hydroxyperoxide groups with a wide peak at 3300–3500 cm−1 triggered by PE’s structural decomposition [47]. Furthermore, the expansion of peak 1712 cm−1 marks the first signs of oxidation of PE’s long carbon-carbon chains [48].
In addition to the changes in functional groups, the UV aging process can lead to textured surfaces [49] and even contribute to the generation of smaller-sized particles, increasing the potential to interface with cellular membranes disrupting normal functions [49,50,51]. Although not proven in this study, previous studies showed that hydrophobicity of most plastic particles, including PE commonly applied as mulch films [52], tend to change with surface morphological and chemical alterations induced by various weathering forces, therefore altering their behavior, movement, and compatibility with certain soil material or other contaminants as they age [8,53,54]. Given the degradation MPs experience under UV irradiation and the prevalence of such in agricultural soils we tested the influence of virgin and photoaged PE on cosmopolitan soil mesofauna, hypothesizing that photoaged particles would induce greater effects with increasing concentrations.
When considering photoaged PE MP particles, our data revealed slightly exacerbated responses in survival and reproduction, which emerged as decreases in survival with corresponding increases in reproduction for P. minuta and to a lesser extent E. crypticus, yet the opposite trend was seen for F. candida with higher survival among photoaged compared to virgin PE MP exposures coupled with reduced reproduction. Despite the lack of NOEC/LOEC, one can deduce that in concentrations up to 200 mg/kg most of the effects were detected, which is in fact the HC5 of PE MPs in soil systems (derived as 202.84 (73.70–558.22 mg/kg soil) [31]). For photoaged MPs, other experiments have been conducted on mainly aquatic species [55,56,57,58]. Aged microplastic exposures on soil species are more limited [12,14,15], while reproduction and mortality are rarely assessed. E. crypticus fed oats spiked with 0.5% soil aged polypropylene experienced a decrease in reproduction after 7 days, compared to pristine polypropylene exposure, yet mortality remained unaffected in either exposure [59]. Additionally, although in an aqueous medium, pristine and UV-photodegraded PS MP (100 μg/L) caused reproductive toxicity in soil species C. elegans, but significantly even more so in photoaged PS MP [10]. Both studies can be comparable to our mildly reduced reproduction in F. candida incubated with photoaged PE MP, but do not track the increase in reproduction seen among P. minuta and E. crypticus incubated with photoaged PE.
The differences in reproduction and mortality seen amongst virgin and photoaged PE MP exposures between individual species in the present study were not as apparent as the interesting differences seen between each species tested, where decreased survival and increased reproduction presented in P. minuta and E. crypticus and an opposite trend emerged for F. candida. The differential effects and responses seen in this study between mesofauna species have been supported in other works [31,60]. Specifically for collembolans, F. candida and P. minuta, variable tolerance is most likely due to their different life histories, functional groups and ultimately physiology [61,62,63]. Our study presented that collembola exposure to each virgin and photoaged PE MP caused F. candida to be slightly inhibited in reproduction while adult survival was maintained, whereas P. minuta adult survival declined while reproduction increased and significantly more so with photoaged PE MP versus virgin. Lin et al. [13] saw similar results in a field plot PE MP addition, with a reduction in abundance of some mite species as opposed to others based on their feeding strategies, trophic level, and overall life histories [64]. Concordantly, it is prevalent in ecotoxicological literature that when F. candida and P. minuta are tested side by side there is variable sensitivity [61,65]. In the present study, it looks as though P. minuta invests in reproduction over survival, and the opposite is true for F. candida although to a lesser extent. These variable tolerances between species to MP exposures could be adaptive forms of stress management through energy allocation [66].
Soil strata inhabitance and activity are also implicated as a primary factor influencing pollutant sensitivity [62,67]. The closer to aboveground dwelling lifestyle for collembolans the more there has been a correlation with increasing sensitivity [68,69,70]. This could explain P. minuta’s overall greater responses, being a hemiedaphic species inhabiting the topsoil, compared to the deeper dwelling euedaphic species F. candida. Further, the fact that E. crypticus adaptively has the means to move along the soil column when conditions are not favorable [71], they may feel less pressed to respond in terms of energy costs to contamination. This may be why less of a response in the survival and reproduction of E. crypticus in the face of sub-lethal low contamination was observed.
This is the first article assessing apical endpoints on multiple soil fauna that compares the exposures of virgin and photoaged PE MPs, which provided highly variable results, both stimulatory and inhibitory. Suppose survival or reproduction is stimulated or inhibited in one species or another; in that case, this is still a departure from the homeostasis of the ecosystem and could lead to a die off of local populations if reproduction is consistently lowered, or overcrowding and breach of carrying capacity, resulting in competition and resource management issues, taking nutrients from other flora and fauna species and threatening the balance in a productive soil environment. Crucially, this study provided an integrative comparison of PE MPs effects across three ecologically relevant soil invertebrate species, using realistic conditions of environmental plastics (photoaged) under a broad range of concentrations (from environmentally realistic to potentially stressful ones). This approach provides valuable insights into species-specific sensitivities, which are critical for improving ecological risk assessment frameworks for terrestrial MPs pollution, an understudied area of research compared to aquatic systems. Therefore, it is important that further research of MPs focuses on how long-term environmental weathering could affect soil organisms for a better understanding of the fate of PE MPs and ecological impacts.

5. Conclusions

E. crypticus experienced a modest reduction in survival yet promotion in reproduction after exposure to photoaged PE MP, contrastingly F. candida had enhanced survival and diminished reproduction when exposed to both PE MP types. Yet only P. minuta showed significant changes in survival and reproduction with decreased survival rates when incubated with both virgin PE MP and photoaged PE MP at 2000 mg/kg and 20 mg/kg, respectively, and increased reproduction when incubated with photoaged PE MP at 200 mg/kg. Our results suggest that PE MP can affect soil mesofauna in variable manners. Environmentally relevant concentrations of PE MP may not be toxic to all soil mesofauna in this brief period of exposure per se, but we did see more profound responses to photoaged PE MP compared to virgin PE MP indicating that UV irradiation can more quickly lead to population shifts among soil mesofauna, and because of the overwhelming probability of MPs becoming irradiated in the environment, especially in agriculture (e.g., PE mulch films), there is a great need to explore further impacts of weathered and aged MPs on soil organisms in cultivated soils on longer timescales.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/environments12060175/s1, Table S1: Soil physiochemistry.

Author Contributions

Conceptualization, J.P.S., S.C. and M.J.I.B.; methodology, J.P.S., S.C. and A.L.P.S.; validation, J.P.S., A.L.P.S. and M.J.I.B.; formal analysis, E.Q. and A.L.P.S.; investigation, E.Q. and S.C.; resources, J.P.S. and A.L.P.S.; data curation, E.Q.; writing—original draft preparation, E.Q.; writing—review and editing, E.Q., A.L.P.S., J.P.S. and M.J.I.B.; visualization, E.Q. and A.L.P.S.; supervision, J.P.S.; project administration, J.P.S. and S.C.; funding acquisition, M.J.I.B. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the SOPLAS project financed by the European Union H2020 Marie Skłodowska-Curie Innovative Training Networks (H2020-MSCA-ITN-2020) under grant agreement No. 955334.

Data Availability Statement

Data available upon request.

Acknowledgments

Thank you to Camila Campello and Patrícia Ferreira for help in experimental setup.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Abbreviations

The following abbreviations are used in this manuscript:
MPsMicroplastics
PEPolyethylene
UV
OM		Ultraviolet
Organic Matter
FTIR
PS		Fourier-transform infrared spectroscopy
Polystyrene

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Environments 12 00175 g001
Figure 1. The FTIR-ATIR spectra of both virgin (P48) and photoaged (UV48) PE MPs in the range of 400–4000 cm−1 (n = 3).
Figure 1. The FTIR-ATIR spectra of both virgin (P48) and photoaged (UV48) PE MPs in the range of 400–4000 cm−1 (n = 3).
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Environments 12 00175 g002
Figure 2. Virgin and photoaged polyethylene microplastics (PE MPs) on survival (# adults) of (A) Enchytraeus crypticus, (B) Folsomia candida, and (C) Proisotoma minuta, after 28 d of exposure. Data reported as average ± standard deviation of the mean (n = 4). (*) denotes statistical differences against control for PE MP concentration as variable.
Figure 2. Virgin and photoaged polyethylene microplastics (PE MPs) on survival (# adults) of (A) Enchytraeus crypticus, (B) Folsomia candida, and (C) Proisotoma minuta, after 28 d of exposure. Data reported as average ± standard deviation of the mean (n = 4). (*) denotes statistical differences against control for PE MP concentration as variable.
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Environments 12 00175 g003
Figure 3. Virgin and photoaged polyethylene microplastics (PE MPs) on reproduction (# juveniles) of (A) Enchytraeus crypticus, (B) Folsomia candida, and (C) Proisotoma minuta, after 28 d of exposure. Data reported as average ± standard deviation of the mean (n = 4). (*) denotes statistical differences against control for PE MP concentration as variable.
Figure 3. Virgin and photoaged polyethylene microplastics (PE MPs) on reproduction (# juveniles) of (A) Enchytraeus crypticus, (B) Folsomia candida, and (C) Proisotoma minuta, after 28 d of exposure. Data reported as average ± standard deviation of the mean (n = 4). (*) denotes statistical differences against control for PE MP concentration as variable.
Environments 12 00175 g003
Table 1. Changes in pH (KCl) and water content (WC) of natural Freixo soil before (0 d) and after (28 d) PE particle exposure (virgin and photoaged) at each concentration treatment, 0 (C0), 0.2 (C1), 2 (C2), 20 (C3), 200 (C4), and 2000 (C5) mg kg−1 (n = 4). Mean ± SD.
Table 1. Changes in pH (KCl) and water content (WC) of natural Freixo soil before (0 d) and after (28 d) PE particle exposure (virgin and photoaged) at each concentration treatment, 0 (C0), 0.2 (C1), 2 (C2), 20 (C3), 200 (C4), and 2000 (C5) mg kg−1 (n = 4). Mean ± SD.
pHWC
BeforeAfterBeforeAfter
PristineC04.97 ± 0.024.94 ± 0.0518.31 ± 1.1517.68 ± 0.97
C15.01 ± 0.694.93 ± 0.0720.14 ± 2.5418.5 ± 0.78
C25.07 ± 05.07 ± 0.1616.72 ± 0.7116.67 ± 0.5
C34.88 ± 0.074.85 ± 0.1317.93 ± 1.217.59 ± 2.8
C44.97 ± 0.054.87 ± 0.0318.18 ± 2.0216.82 ± 1.56
C55 ± 0.034.92 ± 0.0517.98 ± 1.0218.96 ± 2.83
UVC04.96 ± 0.064.85 ± 0.0619.39 ± 015.48 ± 2.36
C14.92 ± 0.0064.83 ± 0.00518.39 ± 015.29 ± 1.06
C24.95 ± 0.034.88 ± 0.0320.21 ± 016.75 ± 1.06
C34.94 ± 0.034.88 ± 0.0324.73 ± 018.12 ± 0.75
C44.92 ± 0.014.85 ± 0.0120.99 ± 016.36 ± 1.46
C54.96 ± 0.044.9 ± 0.0418.95 ± 016.6 ± 1.06
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Quigley, E.; Patrício Silva, A.L.; Chelinho, S.; Briones, M.J.I.; Sousa, J.P. Virgin and Photoaged Polyethylene Microplastics Have Different Effects on Collembola and Enchytraeids. Environments 2025, 12, 175. https://doi.org/10.3390/environments12060175

AMA Style

Quigley E, Patrício Silva AL, Chelinho S, Briones MJI, Sousa JP. Virgin and Photoaged Polyethylene Microplastics Have Different Effects on Collembola and Enchytraeids. Environments. 2025; 12(6):175. https://doi.org/10.3390/environments12060175

Chicago/Turabian Style

Quigley, Elise, Ana L. Patrício Silva, Sónia Chelinho, Maria J. I. Briones, and Jose P. Sousa. 2025. "Virgin and Photoaged Polyethylene Microplastics Have Different Effects on Collembola and Enchytraeids" Environments 12, no. 6: 175. https://doi.org/10.3390/environments12060175

APA Style

Quigley, E., Patrício Silva, A. L., Chelinho, S., Briones, M. J. I., & Sousa, J. P. (2025). Virgin and Photoaged Polyethylene Microplastics Have Different Effects on Collembola and Enchytraeids. Environments, 12(6), 175. https://doi.org/10.3390/environments12060175

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