Environmental Science and Pollution Research (2024) 31:51747–51759

https://doi.org/10.1007/s11356-024-34615-w

RESEARCH ARTICLE

Analysis of microplastics in the reuse of compost in three agricultural

sites (Cádiz, Spain) as a circular economy strategy: detection
of micropollutants and incidence of plastic ingestion levels
by annelids
Ayda Sakali1 · Agata Egea‑Corbacho1 · Dolores Coello1 · Gemma Albendín2 · Juana Arellano2 ·
Rocío Rodríguez‑Barroso1

Received: 1 March 2024 / Accepted: 30 July 2024 / Published online: 10 August 2024
© The Author(s) 2024

Abstract
The system of fertilizing agricultural soils with sludge or compost from wastewater treatment processes, as one of the principles
of the circular economy, can lead to microplastic (MP) contamination. The existing technical standards for fertilization are very
recent and do not consider this problem, although there is scientific evidence of their existence. Therefore, this study, on the one
hand, evaluates the presence of MPs in agricultural soils, previously treated with sludge or compost from wastewater treatment
plants for fertilization, and on the second hand, it studies the effect of these MPs on earthworms in three different locations in the
south of Spain. For the study, selected composts deriving from the different stages of the composting process and three fertilized
soils with increasing MP doses were followed. Samples were taken from different sections in depth (0–5, 5–10, and 10–20 cm) to
study the shape, size, type, and abundance of MPs using infrared spectroscopy (FTIR). The results showed that the most abundant
shape was fiber, followed by fragment and finally bulk, for both composts and soils. Regarding size distribution, 100 µm was
the predominant size in composts (64.3% ± 9.8), while in the case of soils, the predominant range was from 100 to 500 µm. The
prevalent polymers in both, composts and soils, were PTFE, TPE, PP, and PET, with four times higher amounts in composts than
in soils. Ingestion of common MPs were also verified in two earthworm species, which ingested concentrations higher than 2.1%
w/w. PP was the most ingested MP and Eisenia fetida was more voracious compared with Lumbricus terrestris. Therefore, it can
be considered a suitable bioindicator for monitoring microplastic contamination in agricultural soil.

Keywords Microplastics · Compost · Southern Spain · Soil · Annelids · PTFE

Nomenclatures LT  Lumbricus terrestris

EF  Eisenia fetida PAHs Polycyclic aromatic hydrocarbons
EPS Extracellular polymeric substances PCBs Polychlorinated biphenyls
FTIR Infrared spectroscopy PC  Polycarbonate
H2O2 Hydrogen peroxide PE  Polyethylene
MPs  Microplastics PET Polyethylene terephthalate
PHDA Poly (hexadecyl acrylate)
PP  Polypropylene
Responsible Editor: Kitae Baek PS  Polystyrene
Highlights
PTEs Potentially toxic elements
The prevalent polymers in both composts and soils were PTFE, PTFE  Polytetrafluoroethylene
PET, PP, and TPE. PVC Vinyl polychloride
PP was the most ingested MPs by worms. SDGs Sustainable Development Goals
Particle size influences feeding habits on worms.
Eisenia fetida was more voracious compared to Lumbricus terrestris.
TPE Thermoplastic elastomers
Worms as bioindicators for monitoring microplastic contamination WHC Water retention capacity
in agricultural soils. WPO Wet oxidation peroxide
WWTP Wastewater treatment plants
Extended author information available on the last page of the article

Vol.:(0123456789)

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51748 Environmental Science and Pollution Research (2024) 31:51747–51759

Introduction do not remove them but can retain and concentrate them in
the sludge line (Egea-Corbacho et al. 2023; Dronjak et al.
Plastic container waste has increased rapidly with home 2023). Preliminary screens and grit chambers remove large
learning and teleworking caused by COVID-19 (Haddad debris, gravel, and sand. Primary treatment removes grease
et al. 2021). Plastics have proven to be a key weapon in and settleable particles (El Mansouri et al. 2022). Secondary
this fight. Degraded physically, chemically, and biologi- treatments in WWTPs include both aerobic and anaerobic
cally, they create small debris, called microplastics (MPs), processes, within the anaerobic ones, and dissolved organic
a catch-all term to describe any water-insoluble solid plastic matter is degraded into carbon dioxide and water (Bilgin
particle between 1 and 1000 µm in size (ISO 2020). MPs et al. 2020) through bioremediation generating gasses such
do not fall directly within the scope of the directive (EU) as methane (Masiá et al. 2020; Huang et al. 2024). Wu et al.
2019/904 of the European Parliament and the Council on the (2020) showed that MP levels might inhibit methane pro-
reduction of certain plastic products’ impact on the environ- duction compared with the negative controls. Another study
ment. However, they contribute to marine litter; therefore, showed the importance of MP size, as nanometer-sized MPs
the European Union should therefore adopt a comprehensive inhibited sludge activity and decreased the abundance of
approach applying to MPs. key microorganisms, which subsequently altered the com-
MPs can be transported from both ocean and land, but position and spatial distribution of extracellular polymeric
their behavior in the soil is still not well-known. Terrestrial substances (EPS) and ultimately prevented sludge dewater-
pollution by polymer items can be significant, on account of ing (Xu et al. 2021).
their high specific surface area as well as their physicochem- The potential for MPs bioremediation in WWTPs is more
ical properties. Moreover, MPs are considered to be vectors evident in the gravitational settling of the sewage sludge.
for other soil contaminants, such as potentially toxic ele- Therefore, the size, toxicity, and type of polymers in the
ments (PTEs) and organic contaminants (Igalavithana et al. sludge must be taken into account, because its accumula-
2022). Several studies mention different toxic compounds tion is not risk-free. Sludge is reused in agriculture with
that can be adsorbed by MPs (Bradney et al. 2019; Thacha- the aim of valorizing a residue according to the principles
rodi et al. 2024), like PAHs, PCBs (Zhang & Chen 2020; of the circular economy (efficiency in the sustainable use
Xie et al. 2024), additives (Edo et al. 2020; Li et al. 2024), of resources), in addition to the fact that it is beneficial to
metals (Li et al. 2021), and neonics (Gross et al. 2022). agriculture; actions aligned with SDGs 14 (Life on land) and
Therefore, the combination of MPs including PTEs can SDGs 12 (Responsible production and consumption). Thus,
help spread toxic effects from one environment to another the appropriate management of sludge should be considered
(Tadsuwan & Babel 2021). The soil as an essential media important to prevent the MP release from WWTPs.
justifies its exploration considering that the occurrence of It is evident that environmental conditions, soil attributes,
MPs can change the living environment of soil fauna, such vegetative cowl, and temporal arrangement of uses sway
as earthworms (Zhang et al. 2022; Tian et al. 2024), and microplastic soil maintenance (Crossman et al. 2020; Tor-
threaten soil properties (Chia et al. 2022). Soil organic car- res et al. 2021). Recent studies related to the identification
bon and total nitrogen stock are called into question since the of MPs in soil revealed that the stabilization of wastewater
additional greenhouse effect coupled with radiative forcing solids, creating end products such as conventional compost
rise the Earth’s energy budget, which is dissipated into the (El Hayany et al. 2020; Vo et al. 2024) or simply dewatered
ground and warms up the atmosphere, leading to heatwaves, sludge (Li et al. 2019), leads to their use as fertilizers (Cor-
organic matter relinquishment, and permafrost crushing, radini et al. 2019; Zhang et al. 2020), and despite efforts to
encouraging the outdoor MP infiltration in the indoor envi- dispose of MPs from WWTPs, a considered percentage still
ronment (Wang et al. 2019). bypasses the removal stage and translocate to soil (Bradney
Wastewater discharges from wastewater treatment plants et al. 2019; Long et al. 2024), from where it is estimated that
(WWTP) are one of the main sources of microplastics from in Europe alone, 125–850 tons of MPs/million inhabitants a
urban agglomerations followed by atmospheric deposition year are added to agricultural soils via sewage sludge applica-
and surface runoff (Zhou et al. 2023). Thus, sewage systems tions (Bank 2022; Mai et al. 2024). Furthermore, it has been
and networks represent an important source of polymers calculated that the average amount of MPs derived from sew-
that transport MPs to WWTPs. In sewer systems, MPs can age sludge that can enter the Spanish soil is 2.80 × ­1014 MPs/
undergo degradation (biotic and abiotic), adsorption, and year (Sakali et al. 2022).
retransformation, but they are not removed in either sewer Deteriorative reactions occur during processing when
networks or WWTPs (Compagni, et al. 2019). WWTPs have polymers, often compared with sediments in a simplified
preliminary, primary, and secondary treatments that are not manner (Waldschläger 2020), are subject to the most important
selective or specific for the removal of MPs and therefore degradative organisms. Forest canopies (Murazzi et al. 2022)

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Environmental Science and Pollution Research (2024) 31:51747–51759 51749

and pine needles (Liu et al. 2022) are also affected and rotten straw and pruning for fermentation (semi-dried com-
evaluated as good receptors of MPs atmospheric deposition. post, C2). The last step consists of conditioning and refining
Earthworms can eventually deteriorate the natural balance the residue by sieving and eliminating the rejects (fine com-
of agricultural systems as they are involved in important post, C3). A representative sample (~ 1 kg, mean moisture
ecological processes such as ammonization, nitrification and content 7.48 ± 4.54%) of each compost type was collected
denitrification (Shen et al. 2022). and frozen as soil samples until analysis. With the help of a
The unpredictable presence of harmful polymers that per- sludge management company in the region (Grupo Valora),
sist in terrestrial ecosystems, as well as their capacity to absorb two types of sludge-enriched soils and one control soil were
pollutants and the difficulties in detecting them, can generate selected from different locations in the province of Cádiz.
potential effects on soil and organisms, which is the focus of this
study. Therefore, in order to prevent MPs from entering the eco- S1: a field with less than 2 years of fertilization (at the
system, more specifically the soil, and generating the problems highest dose 30 t/ha) plowed twice/year (36° 44′ 40.38″
mentioned above, more studies are required to understand their N; − 6° 20′ 57.12″ W).
inclusion arrival and behavior in the environment. In addition, S2: a sunflower field with more than 4 years of fertiliza-
these studies will allow the development of stricter standards tion (at the lowest dose 15 t/ha) plowed twice/year (36°
for both agriculture and sludge management, additionally to the 36′ 51.372″ N; − 6° 10′ 36.84″ W).
improvement of technologies and management strategies, which S3 (Control): a chickpea field without exposure to
results in a great challenge for industry and research (Ivleva sludge (36° 23′ 35.16″ N; − 5° 54′ 16.128″ W).
2021; van den Berg et al. 2020; Meng et al. 2020).
This study is aimed at investigating the presence of MPs A noteworthy fact is that the study examined the same
in agricultural soils that have been previously fertilized with sludge before being composted and after it had been applied
sludge or compost coming from WWTPs. In addition, the to the soil. S1, S2, and S3 were silty clay to clayey textured
ingestion capacity of earthworms will also be evaluated as soils, which are considered good for agriculture, with no evi-
bioindicators. For this purpose, the composition, diversity, and dence of early antiweed netting or temporary greenhouses.
abundance of MPs in three composts derived from convention- From each soil, four random sampling points were collected
ally treated sludge throughout the composting process as well and integrated into a single sample. Using a metal soil auger,
as in three sludge-enriched soils were investigated. Also, two S1 and S2 samples were first taken from the topsoil layer (0–5
types of earthworms were studied as possible bioindicators cm), followed by the middle layer (5–10 cm) and finally the
to check the level of ingestion at increasing doses of the most deep layer (10–20 cm). These depths were selected to evaluate
common MPs found (0.9, 2.1 and 3% w/w). the polymer content in the root zone. Previously, each sample
To monitor MP levels, we developed a method for the (~ 300 g, mean moisture content 0.58 ± 0.37%) was sieved,
MPs analysis, by using infrared spectroscopy (FTIR) to in situ, through a stainless mesh < 5 mm ø to avoid any possible
identify polymer features and provided evidence to confirm coarse branches or residues. All soils experienced similar
that sludge and compost are relevant land-based sources of edaphic conditions; the average temperature recorded was
MPs in the agrosystems. It is hypothesized that the abun- 23.44 °C, ranging from a minimum of 22.4 °C to a maximum
dance and size of MPs in agricultural soils may increase of 25 °C. The average relative humidity was 78.58% and varied
with increasing fertilization and composting stage. between 70 and 88%. The wind, mainly westerly, blew at an
average speed of 5.66 m/s (20.38 km/h), and a maximum gust
of 14 m/s (50.4 km/h). S3 was the only soil where its layers
Materials and methods were combined prior to lab analysis, because as a control soil,
there was no record of sludge application.
Sample collection
Laboratory analysis
The analyzed compost comes from a plant located in Southern
Spain, owned by the company Valoriza Medioambiente Compost samples were treated as sludge according to Sakali
(SACYR). It combines sewage sludge and vegetable et al. (2021, 2022), based on an ­H2O2 protocol, commonly
biomass from municipal parks and gardens, obtaining as a known as wet oxidation peroxide (WPO), followed in
final product an organic fertilizer with very good agronomic sequential time steps to extract the MPs by flotation.
characteristics, mainly suitable for agricultural use. It has been reported that standard separation methods for
In general terms, the composting process consists of MPs from the soil are deficient (Li et al. 2019) and that most
spreading sewage sludge over drying beds for a few weeks at are under consideration (Li et al. 2021; Yu & Flury 2021).
ambient temperature (humid compost, C1). Then, the sludge Therefore, we implemented a methodology based on Zhang
is piled up, mixed with other by-products such as manure, et al. (2020) study (Fig. 1), in which the soil samples were

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51750 Environmental Science and Pollution Research (2024) 31:51747–51759

Fig. 1  MP separation method from the soil

pretreated to homogenize and disaggregate, avoiding any respect to registered concentrations in natural soils, and
agglomeration. Roughly, 5 g of each substrate was processed therefore, further studies with lower MP concentrations
with ­ZnCl2 hypersaline solution (100 mL, ITW Reagents) should be followed.
on a digital hot plate (Ovan, Spain) at 8 rpm for 30 min. Two tests were carried out, a preliminary test with a
One hour sample settling was required. ­ZnCl2 separation substrate conditioned for worms, supplied by a local com-
was repeated three times to reach maximal particle range mercial supplier (Centro de Energía Viva de Andalucía,
flotation. The supernatants were recuperated with a 25-mL CEVA), which was previously analyzed in means of MP
pipette then dropped on three 8-in diameters, 500-, 100-, and content according to the exposed methodology for soils,
63-µm stainless steel sieves, moved into clean glass beakers. under controlled laboratory conditions (named preliminary
Repeated rinsing of the sieve with ­H2O2 (30%) was necessary trials), and then a second test following the same proce-
to recuperate every particle. Thereafter, ­H2O2 (100 ml, ITW dure, but this time with a real soil, containing the highest
Reagents) was added to react with final supernatants for 72 concentration of MPs (S1) (named agricultural field trial),
h at 60 °C, 8 rpm. The samples were sieved, washed with which was preconditioned with water.
ultrapure water, and then, filtered through polycarbonate Two polymers that were identified in the sample soils
filters (PC) (47 mm ø, 0.8 μm, Isopore™) by a vacuum (polyethylene terephthalate (PET) and polypropylene (PP))
pump and dried for 2 h at 40 °C to pursue microscopic in addition to PS (polystyrene) were used. These were, pre-
identification. viously ground as bulk shape to the average size identified
A negative control next to each soil and compost sample in this study. For the study, the following plastic materials
was included so there would be no compromising the quality with known composition, such as plastic straws (PP), plastic
of the analysis. The controls enclosed clean, empty beakers spoons (PS), and cork (PET), were used. Sample of about
that were placed adjacent to the ones containing the actual 40 g of each material were crushed to a size larger than 5 mm
samples and were processed the same way. All materials and then crushed into a much smaller size ranged between
employed in the laboratory analysis were made of glass and/ 100 and 250 µm with the help of a Retsch Ultra Centrifugal
or stainless steel. Mill ZM 200, USA (IVAGRO (Instituto de Investigación
Vitivinícola y Agroalimentaria)) based on liquid nitrogen.
Earthworm trials Prior to their use in testing, the materials were analyzed
by FTIR to confirm and check the initial materials of the
In order to analyze possible ingestion of MPs by crushed elements, after the first crushing and grinding. In
characteristic organism of the agricultural soil fauna all three cases, the FTIR yielded the same information and
(earthworms), an experiment was designed based on the confirmed the existence of the reference polymers PET, PP,
study followed by Baeza et al. (2020). The aim of this and PS compared with the commercial polymers available
experiment was to evaluate if the type of MPs identified in in the laboratory.
agricultural soils and its average size (ø < 250 μm) could Two types of worms, sourced from the same commer-
be ingested. Therefore, two types of worms (Lumbricus cial supplier, were investigated Lumbricus terrestris (LT)
terrestris (LT) and Eisenia fetida (EF)) were exposed to and Eisenia fetida (EF). All experiments in this study were
different MP types in increasing concentrations (5, 7, and followed with adult earthworms (LT 5.1 ± 0.7 g and EF
10%), in reference to previous results showing that higher 2.7 ± 0.7 fresh weight). During the period of adaptation to
concentrations affect organisms negatively. However, the laboratory conditions (approx. 1 month), the earth worms
selected concentrations in this study could be too high in were kept alive by adding crushed apples as food. Prior to

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Environmental Science and Pollution Research (2024) 31:51747–51759 51751

the test, the worms were conditioned by emptying their Instruments and analytical conditions
intestine; hence, they were placed on wet filter paper for 24
h. In this way, the worms increased their appetite for soil The filters with the recovered particles were examined by
and encouraged their digging into the soil (Lahive et al. a stereomicroscope (ZEISS Achromat S 1.25 × FWD 50
2022). mm, UK) equipped with a digital ZEISS Axio camera. The
For both types of worms, a control (without MPs in soil) observed items were classified as fiber, bulk (granular), or
in addition to three trials was carried out where the soil was fragment (irregular shape particle) according to their mor-
mixed with the MPs in increasing concentrations of 0.9, 2.1, phologies. The size was measured using the included soft-
and 3% w/w. For each exposure, four mature worms (with ware, divided into the same range of sieves. The polymer
a visible band about 1/3 or less down from the top) were type was identified in total attenuated reflection mode with
placed. The eight different trials were carried out in glass a Fourier transform infrared (FTIR) spectrometer (Spectrum
receptacles (Imhoff cones, India) to maintain a soil column 100™, PerkinElmer, USA) (Sakali et al. 2021).
of about 20 cm (Fig. 2) and reproduce similar field condi-
tions in the dark (with the use of rubbish bags). Quality control measure
Table 1 shows the amounts (g) of soil and MP exposures,
in addition to the number of individuals (worms) of each Monitoring contamination throughout the process is an impor-
type. These trials were maintained for a period of 7 days, tant fact for the analysis of MPs. Attention should be paid to
after which the worms were individually extracted for sub- implementing consistent QA/QC practices from inception
sequent MP analysis according to the protocol established through the entire study process (including during the design
by Zhang et al. (2020), which employs prior digestion of of the study, sampling and collection process, extraction, and
the individuals, followed by a sieving process to retain the analysis). Cotton clothes and gloves were worn during sam-
microparticles on PC filters. pling and analysis to avoid contamination by plastic fibers.

Fig. 2  Earthworms’ bioassays:

a mimic soil conditions, b
samples in darkness, c after MP
exposure

Table 1  MP concentrations in Samples Soil (g) MPs (g) Earthworms

each worm trial (Nº of individuals)
PP PET PS LT EF

LT1 (0.9% w/w) 300 1.5 1.5 1.5 4 4

LT2 (2.1% w/w) 300 3.5 3.5 3.5 4 4
LT3 (3% w/w) 300 5 5 5 4 4
Control 1 (C1) 300 0 0 0 4 4
EF1 (0.9% w/w) 300 1.5 1.5 1.5 4 4
EF2 (2.1% w/w) 300 3.5 3.5 3.5 4 4
EF3 (3% w/w) 300 5 5 5 4 4
Control 2 (C2) 300 0 0 0 4 4

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51752 Environmental Science and Pollution Research (2024) 31:51747–51759

During the experiment, controls of both aerial blanks, (Fig. 3a). This is in line with other studies, which mentioned
soil, and compost samples that formed the substrate for the that these are the most abundant in compost (Braun et al.
earthworms were carried out. Mainly acrylic, cellulose, and 2020; Edo et al. 2022). The large amount of fibers can be
polyester fibers of 0.2 to 3 mm in length were found. There- attributed mainly to their release of fibers from the textile
fore, these types of polymers were excluded from the results industry and the washing of synthetic garments (Henry et al.
due to a possible source of laboratory contamination. 2019; Cohen et al. 2021), while in the case of fragments,
The data obtained were reported starting with shape, size, they usually derive from secondary MPs due to the fragmen-
type, and abundance of MPs in compost and then soil, ending tation of larger particles (Nguyen et al. 2019). The bulk form
with an overall comparison between both earthworm species. was found in smaller proportions (Fig. 3d), with an 11% in
C1, a 9% in C2, and 21% in C3 (Fig. 3a).
The behavior of particles during the composting process can
Results and discussion be well described by monitoring the evolution of their size.
Figure 3b indicates that for all three types of compost, micro-
Presence of MPs in the compost samples particles of 100 µm predominated, especially in C1 and C2. The
possible explanation is that small-sized MPs tend to overlap
Fibers and fragments resulted to be the most abundant. Fib- easily due to mass and remain entrapped in the sludge. How-
ers were, on average, 5 times more abundant than fragments. ever, in C3, the difference in microparticle size was smaller.
Overall fibers were nonwoven, with much higher elongation, This apparent distinction in the particle size can probably be
and had an average length of 982.6 µm compared with the ascribed to the application amount of sewage sludge and the
overall average fragment of 176.9 µm. application history. The highest number of 100 µm micropar-
An increase in the number of microparticles during the ticles was found in C2 reaching values of up to 150.1 ± 36.1
composting process was also observed, resulting in 286 particles/g, while in C3, the highest number referred to 500 µm
microparticles in C3 compared with C2, with 193 micro- microparticles resulting of 141.8 ± 41.8 particles/g correspond-
particles and C1 with 157 microparticles. ing to 71% and 33%, respectively (Fig. 3b).
In reference to the fibers and fragments presence, in the Curiously, the percentage of particle quantity increased
case of C1, fibers reached an average of 63% and fragments during the composting process, the compost with the high-
of 26%; in C2, they represented a 60% and 31% respectively; est number of microparticles was the finest with a total of
and in C3, the fibers reached 54% and the fragments 25% 285.7 ± 30.4 particles/g. This may be due to the fact that,

Fig. 3  Morphotype (a), size dis-

tribution (b), polymer type (c),
and photos of MPs shape found
in the compost samples (d)

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Environmental Science and Pollution Research (2024) 31:51747–51759 51753

during the composting process, there was some external

atmospheric contamination. Therefore, more 500 µm micro-
particles were found compared with all other types of com-
post which is similar to the results obtained by EL Hayany
et al. (2020). In the case of C3, this could be from mixing
C1 with shrub pruning and branches, which is a way plastic
becomes incorporated (Jiao et al. 2024).
In this way, although the collected sewage sludge that
is used as agricultural amendment and soil compost
(Koyuncuoğlu & Erden 2021) is considered to be a valu-
able and economic mineral product, this is still in question
because it is not free of MPs. Via FTIR, an average of 56%
of the samples were confirmed as plastic during chemical
analysis. Poly (hexadecyl acrylate) (PHDA), polyethylene
(PE), polyethylene terephthalate (PET), and polypropylene
(PP) were identified among the potentially plastic-derived Fig. 4  Distribution of particles in the soils (S1, S2, and S3) and
spectroscopy products; inert polymers were also found, i.e., depths studied (topsoil (0–5 cm), middle layer (5–10 cm), and deep
polymers that hardly react with external agents such as PTFE layer (10–20 cm))
and others shown in Fig. 3c.
An hypothesis did stand up with respect to the by-prod- for fibers, 23% ± 11.0 for bulk particles, and 20% ± 1.6
ucts for fermentation of C2, which may have stimulated deg- for fragment. Fiber contamination decreased depth unlike
radation and loss of organic carbon or added MPs, such as that of bulk. It is important to highlight that fragment
what happened with PHDA. distribution showed the same particle mobilization in the
During the C3 step, PTFE (fragments and fibers) and TPE middle and deep layers. A completely different trend of
(overall fibers) demonstrated large increases compared with particle distribution was observed in S2, showing lower
C2, probably due to the mechanical conditioning and refin- particle abundance than in S1; the morphotypes of fiber
ing of the residue before the sales service. and bulk had the greatest proportion in the middle layer,
The MP abundance which attained 171.2 ± 8.3 × ­103 MPs/ while fragments predominantly accounted for 63% ± 27.1
kg (dw) in the final stage of C3 resulted in the same order of in the deep layer. In all cases, the topsoil was positioned
magnitude as other studies, which reported that MPs con- in second place of item retention. The possible explana-
centrations range from 23.0 ± 5.7 × ­103, 26.0 ± 8.3 × ­103, and tion is that S2 with the biggest amount of particles, as
18.0 ± 3.2 × ­103 particles/kg, respectively, in Morocco’s final was expected since it is the soil with more than 4 years of
composts (EL Hayany et al. 2020), 10–30 items/g in north- sludge exposure, was pushed towards the bottom (10–20
ern Spanish dry compost (Edo et al. 2022), and 200 − 420 cm) due to a downward mechanical movement during the
items/kg with an average of 353.3 ± 97.0 items/kg in Chinese soil plowing process which tended to an accumulation in
composts (Zhang et al. 2020). the middle deep layers in contrast to the topsoil (0–5 cm).
S3 showed enrichment of fiber and fragment even though
Presence of MPs in agricultural soils there was no record of sludge exposure, apparently; there
is previous evidence that atmospheric fallouts can promote
The average particle distribution (%), within standard their accumulation anywhere (Bianco & Passananti 2020;
errors, was calculated for 28 samples in total. Results Evangeliou et al. 2020; Zhang et al. 2020).
showed that all soil samples contained more fibers (from For the three soils studied, the size distribution in Fig. 5
37% ± 14.8 to 66% ± 11.8 in all layers) than fragments (mean, shows that nearly two-fifths (42.5% ± 7.8) of the particles
28.5% ± 17.7), which results is in line with similar studies were larger than 500 µm and only 19.3% ± 4.8 were big-
(Corradini et al. 2019; Li et al. 2019; Schwinghammer et al. ger than 63 µm on average in all soil layers, which is in
2020; Crossman et al. 2020; Zhu et al 2021). However, Zhang line with previous studies (Yu et al. 2021; van Schothorst
et al. (2020) only found a fiber dominance in fields that had et al. 2021; Zhang et al. 2020). Also, particles bigger than
never plowed nor irrigated with wastewater. In addition, van 500 µm were also abundant in the topsoil and account for
den Berg et al. (2020) explained the existence of a preference 50% of S1. S3 demonstrated a significant net of particles
for fragments to be retained in the soil, rather than fibers. (> 500 µm) equal to 45%. In addition, medium-sized parti-
Particle distribution varied significantly, between soils cles (> 100 µm) had a remarkably higher percentage (42%)
and depths. As shown in Fig. 4 in the case of S1, there in the topsoil layer than bigger particles (35%) in the case
was a particle distribution with mean values of 57% ± 11.8 of S2. Size distribution has also been scrutinized in other

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51754 Environmental Science and Pollution Research (2024) 31:51747–51759

Fig. 5  Size distribution in each

layer (MPs/g dw) area distribu-
tion in the soils (S1, S2, and S3)
for the topsoil (0–5 cm), middle
layer (5–10 cm), and deep layer
(10–20 cm)

urban settlements and was dominated by < 50 µm sized preference for 63 µm < particles < 100 µm with high percent-
particles in India (Sarkar et al. 2022) and < 250 µm in the ages, which may be related to soil density, surface runoff,
Netherlands (Cohen et al. 2021). This difference in size recent plowing, or fauna burrows making (Yu & Ma 2020).
composition implies that some particles may have been Chemical identification of microparticles by FTIR con-
decaying in nature for extended periods of time. Also, the firmed that a mean, 45%, are indeed MPs. Soil samples
sludge can transport suspicious particles into the soil that showed a wide variety of them. Figure 6 shows the number
filter their toxic effects in depth (Milojevic & Cydzik‐ of MPs per gram obtained for each soil sample according to
kwiatkowska 2021). size fractions. Expressing size distribution this way, instead
No significant depth-dependent differences in particle of by percentage, shows slight difference depending on of
size were observed within the other two layers left in S1. 100 and 500 µm, which was not appreciated when displayed
In this way, particles bigger than 500 µm remained similar as percentage unity.
in all layers. In the case of S2, the 100 and 500 µm parti- PTFE dominance in the topsoil could be owed to the
cles matched results in the middle layer, achieving a 40%, fact that it is an inert polymer originated from the wash of
showing a tendency to dominance of larger particles in the daily Teflon utensils, while TPE dominance can be related
deep layer (44%). The distribution of particles smaller than to car tyres or building insulation. In fact, the most abundant
63 µm in S1 was as follows: 18% in the topsoil, 19% in the polymer, overlapped in all layers, is PTFE, which scores
middle layer, and 10% in the deep. In the case of S2, these 54.8 MPs/g dw. This polymer has many applications such as
particles resulted predominant and accounted for 25% in the thread for sewing products that are continuously exposed to
deep layer showing a slightly drop off with decreasing depth, atmospheric and/or chemical agents. It is also used in agri-
while S3 scored 20% even without plowing. cultural irrigation systems to prevent water leaks in pipes or
The achieved results revealed that the particle size dis- stopcocks, and it is found in textile products (Seymour and
tribution in both S1 and S3 was distorted; in contrast to Yu Carraher 2002). The second most abundant polymer in the
et al. (2021), only the deepest layer in S2 showed a retention soil samples was PP (31.8 MPs/g dw), probably because of

Fig. 6  Type of MPs in each layer (MPs/g dw)

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Environmental Science and Pollution Research (2024) 31:51747–51759 51755

its many industrial applications including electrical and elec-

tronic components, industrial materials, vehicle parts and
components, packaging, cosmetics, and medicines (Seymour
and Carraher 2002; Mukherjee et al. 2023). In addition,
other studies also showed that these polymers appeared with
an average abundance of approximately 15% (Bayo et al.
2020). In our study, the percentages are somewhat differ-
ent (Fig. 6). PTFE corresponds to 34.9% of the MPs found
and PP to 20.2%, which is not in similitude with the MPs%
transfer from biosolids to the soils of agricultural fields to
which they were applied, in Ontario, Canada (Crossman
et al. 2020).
Therefore, the results obtained in this study showed that Fig. 7  Typology of polymers found in the examined species
soil subjected to higher doses of fertilization presented a
higher abundance of MPs. Resulting in 58.8 × ­103 MPs/kg
for S2 (with the lowest dose at 15t/ha) versus 84.0 × ­103 and EF3, respectively. Moreover, this invertebrate showed
MPs/kg for S1 (the highest dose at 30 t/ha), minor abun- more appetite for PP, followed by PET; however, there was
dance was registered by S3 (33.3 × ­103 MPs/kg). When com- no evidence of PS ingestion in any of the trials (Fig. 7). In
paring data with literature, these exceeded those of Chile and both controls, the earthworms ingested PP and cellulose,
Canada with an average of 34 × ­103 MP particles/kg (Cor- although the latter was not identified in the experimental
radini et al. 2019) and 11.5 × ­103 MPs/kg (Crossman et al. soils (Fig. 7). Also, the EF species, despite being smaller,
2020), respectively; and wat above those found in China ingested more microparticles per gram than the larger ones.
with an average of 316.75 elements/kg (Zhang et al. 2020). There is previous evidence of the voracity of Eisenia fetida
However, they resulted similar to those found in northern in addition to a high perforation power (Chen et al. 2020).
Spain with an average of 50 × ­103 MP particles/Kg (van den In the case of S1, the soil with the highest contamination
Berg et al. 2020). by MPs, due to its silty-clayey to clayey texture a preparation
with water was necessary before use; therefore, the water
MPs ingestion assays in earthworms retention capacity (WHC) was analyzed (45 ml per 100 g
of soil). However, during the acclimatization period both
After 7 days of exposure, the worms were individually species of worms ended up dying within 7 days, observing
extracted from the soil. Once pulled out they were weighed rigidity and dryness of the worms. This could be due to vari-
and measured, after being thoroughly rinsed and wiped care- ous causes, such as soil acidity due to excess of nitrogenous
fully, showing no differences in weight or length, and all or high protein substances, excess moisture, or even overly
with healthy appearance. dry substrates (Bueno 2015).
Regarding the identification and quantification of the A study on the global distribution of earthworm diversity
types of polymers ingested, both species showed a progres- (Phillips et al. 2019) found that climatic variables and habi-
sive increase in the total content with a rise of exposure to tat cover are more important in shaping earthworm commu-
MPs. Hence, for Lumbricus terrestris, results were of 2.79 nities than soil properties; however, another recent study on
MPs/g body weight for LT1 compared with 5.12 MPs/g of the state of soil degradation (Rodríguez-Berbel et al. 2022)
body weight in LT2 and 7.25 MPs/g of body weight in LT3, considers contamination by microplastics as one of the main
while the control, C1, resulted with 2.3 MPs/g body weight. problems, along with overgrazing, salinization, and the use
Independent from the polymers dosed, the LT worm ingested of agrochemicals.
PS in all 3 trials, although in a very small amount, and two of According to this latest investigation, our data corrobo-
the trials showed the presence of PET. It was observed that rate the presence of MPs in agricultural soils amended with
in the case of PP, the control worms had already ingested compost from sewage treatment plants (with a common size
this polymer, possibly because the soil used for the prelimi- of MPs of < 250 µm in diameter), and this study also con-
nary tests contained it prior to testing, stating an increase firms that earthworms are capable of ingesting them. As
with the dose, being this polymer the most easily incorpo- it can be seen in Fig. 7, results show that a higher dose of
rated during their ingestion (Fig. 7). MPs/g available in the environment result in a higher inges-
The same behavior was registered for Eisenia fetida as tion. Therefore, the doses 3% w/w was the one that showed
the content of microplastics per body weight increased with the highest concentration of MP/g in the individuals for both
the added dose (4.31, 5.53, and 8.93 MPs/g), for EF1, EF2, species of earthworms studied.

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51756 Environmental Science and Pollution Research (2024) 31:51747–51759

Conclusions Author contribution Ayda Sakali: Methodology, investigation, data

curation, writing—original draft. Agata Egea-Corbacho: Writing,
original draft; writing, review and editing. Dolores Coello: Valida-
The study of MP inputs into agricultural soils originat- tion, resources, funding acquisition. Gemma Albendín: Validation;
ing from applied commercial composts or sewage sludge, data curation; resources; writing, original draft; writing, review and
together with the study of the sequential update by soil biota editing. Juana Arellano: Resources, writing—review and editing. Rocío
Rodríguez-Barroso: Conceptualization; methodology; investigation;
is of great importance to understand the fate and transport
data curation; writing, original draft; writing, review and editing.
of MPs in the environment.
The amount of MPs found in the fine compost samples Funding Funding for open access publishing: Universidad de Cádiz/
(S3, control) were 33.3 × ­103 MPs/kg. While in the case of CBUA This research was funded by the Spanish Ministry of Science
and Innovation (RTI2018096771-B-I00) and Aula Universitaria del
the sludge-enriched soil, MPs ranged from 58.8 × ­103 MPs/
Estrecho (AUE, Cádiz) as part of the grant awarded to Ayda Sakali.
kg (S2, the lowest dose at 15t/ha) to 84.0 × ­103 MPs/kg (S1,
the highest dose at 30 t/ha). Data availability The authors declare that data supporting the finding
This study identified compost and sludge as a major solid of this study are available within the paper. If raw data files in another
format are required, they are available from the corresponding author
source of MPs. Moreover, there is a clear increase in the
upon reasonable request.
relationship between the stage in the composting process
and the numbers of particles and MPs increase. Both plowed Declarations
soils studied demonstrated an abundance of MPs in the
middle layer supporting the hypothesis that the abundance Ethical approval Not applicable.
and particle size of MPs (63–100 µm) in agricultural soils
Consent to participate Not applicable.
increase with increasing fertilization and composting stage.
Regarding the micropollutant transition to the worms Consent for publication Not applicable.
embedded in cones, there was hardly any influence observed
Competing interests The authors declare no competing interests.
with respect to the MP dosage in the first trials for both spe-
cies studied (LT1 and EF1). However, we could confirm that
Open Access This article is licensed under a Creative Commons Attri-
the lower the dose of MPs/g available in the environment,
bution 4.0 International License, which permits use, sharing, adapta-
the lower the ingestion. Therefore, the amount of MPs/g tion, distribution and reproduction in any medium or format, as long
detected in both species of earthworms was studied, being as you give appropriate credit to the original author(s) and the source,
the dose of 3% w/w the one that shows the highest concen- provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
tration of MPs/g in the individuals for each species.
included in the article’s Creative Commons licence, unless indicated
We could then consider that from this concentration of otherwise in a credit line to the material. If material is not included in
MPs in agricultural soils, and of the most identified size the article’s Creative Commons licence and your intended use is not
(diameter < 250 µm), a considerable intake by these anne- permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
lids could occur. Regarding the type of MP ingested, PP
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
was found in a higher proportion. When comparing both
species, it turned out that Eisenia fetida showed a greater
voracity than Lumbricus terrestris, due to its higher content
of microparticles per gram of body weight. References
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Authors and Affiliations

Ayda Sakali1 · Agata Egea‑Corbacho1 · Dolores Coello1 · Gemma Albendín2 · Juana Arellano2 ·
Rocío Rodríguez‑Barroso1

2
* Gemma Albendín Toxicology Department, International Campus of Excellence
[email protected] of the Sea (CEIMAR), Faculty of Marine and Environmental
Sciences, University Institute of Marine Research (INMAR),
1
Department of Environmental Technologies, Faculty University of Cádiz, 11510 Puerto Real, Spain
of Marine and Environmental Sciences, INMAR-Marine
Research Institute, CEIMAR International Campus
of Excellence of the Sea, University of Cadiz, Campus
Universitario de Puerto Real, 11510 Cadiz, Spain

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