behaviour of anecics means a vertical transport of APIs towards deeper soil layers,
thus increasing the risk of plant exposure to these compounds via the root system.
For example, some studies have reported that anecic (e.g. L. terrestris) and endogeic
(e.g. A. caliginosa) earthworms facilitate translocation of water-soluble organic
contaminants [59], metals [60], Ag nanoparticles [61] and microplastics [62, 63]
from soil surface to deeper soil layers through the bioturbation process. Moreover,
anecic earthworms could contribute to environmental fate of APIs via the following
three processes: indirect microbial degradation occurring in the burrow walls and
middens, vertical transport of APIs from the soil surface towards the deep soil via
leaching through the burrows and via burying of API-contaminated litter, and
trophic transfer of APIs to earthworm predators (e.g. birds). Past studies with
pesticides [59], metals [64] and more recently with microplastics [65] also lead to
hypothesise that APIs could be lixiviated by the action of earthworms. Likewise, the
high microbial and mesofauna activity and diversity in burrow walls [66, 67] and
middens [54, 68] make them hotspots for API biodegradation. In fact, a wide range
of soil organisms such as springtails, enchytraeids, mites, nematodes and millipedes
are generally found in earthworm casts and in the burrow linings [54, 66, 69].
All three ecological groups of earthworms will contribute to pollutant degradation
in different ways, and the magnitude of this effect largely depends on feeding habits
(litter feeders versus geophagous) and the impact on soil microorganisms, which are
the major drivers of contaminant biodegradation. Furthermore, the burrow system
holds a high microbial activity and biomass [67, 70], which is reflected in the higher
enzyme activity of burrow walls respect to that in undisturbed soils [71–73]. Dissipation of APIs in earthworms’ biostructures (burrow walls, casts and middens) needs
to be further explored to know the impact of both anecic and endogeic earthworms in
the environmental fate of APIs in agricultural soils. Recently, Briones and ÁlvarezOtero [74] reported marked differences in the cuticle and epidermis thickness of the
three ecological groups of earthworms. Anecic species have thickest cuticle
(4.03 Æ 1.6–5.72 Æ 1.7 μm, range of mean Æ SD) and epidermis
(42.7 Æ 16.7–46.3 Æ 9.7 μm) than epigeic (cuticle ¼ 1.51 Æ 0.4–3.21 Æ 1.5 μm,
epidermis ¼ 24.7 Æ 5.2–39.4 Æ 14.5 μm) and endogeic species
(cuticle ¼ 0.46 Æ 0.15–1.22 Æ 0.52 μm, epidermis ¼ 31.1 Æ 7.5–38.9 Æ 10.5 μm).
Beside the taxonomical and ecological meaning, these species-specific differences in
the tegument thickness may be relevant in ecotoxicology. Past studies using
E. andrei as model already demonstrated that the uptake of organochlorine pollutants takes place across the skin and the gastrointestinal epithelium [75]. Using a
three-compartment model (soil-earthworm tissue-gut content), the researchers found
that the uptake of organochlorine compounds via gastrointestinal tract was a significant bioaccumulation route for highly hydrophobic chemicals (log K OW > 6)
[75]. In addition, the transfer across the skin decreased as the K OW value of the
organochlorine compounds increased. Probably, the mucous secretion of skin and
the cuticle layer contributed to reduce the uptake of highly hydrophobic pollutants
through the skin. The role of the cuticle thickness in API bioaccumulation may be
supported by the data in the study by Carter et al. [76]. These researchers compared
the bioconcentration factors and uptake rates of four APIs (carbamazepine,
Vermiremediation of Pharmaceutical-Contaminated Soils and Organic Amendments
347
thus increasing the risk of plant exposure to these compounds via the root system.
For example, some studies have reported that anecic (e.g. L. terrestris) and endogeic
(e.g. A. caliginosa) earthworms facilitate translocation of water-soluble organic
contaminants [59], metals [60], Ag nanoparticles [61] and microplastics [62, 63]
from soil surface to deeper soil layers through the bioturbation process. Moreover,
anecic earthworms could contribute to environmental fate of APIs via the following
three processes: indirect microbial degradation occurring in the burrow walls and
middens, vertical transport of APIs from the soil surface towards the deep soil via
leaching through the burrows and via burying of API-contaminated litter, and
trophic transfer of APIs to earthworm predators (e.g. birds). Past studies with
pesticides [59], metals [64] and more recently with microplastics [65] also lead to
hypothesise that APIs could be lixiviated by the action of earthworms. Likewise, the
high microbial and mesofauna activity and diversity in burrow walls [66, 67] and
middens [54, 68] make them hotspots for API biodegradation. In fact, a wide range
of soil organisms such as springtails, enchytraeids, mites, nematodes and millipedes
are generally found in earthworm casts and in the burrow linings [54, 66, 69].
All three ecological groups of earthworms will contribute to pollutant degradation
in different ways, and the magnitude of this effect largely depends on feeding habits
(litter feeders versus geophagous) and the impact on soil microorganisms, which are
the major drivers of contaminant biodegradation. Furthermore, the burrow system
holds a high microbial activity and biomass [67, 70], which is reflected in the higher
enzyme activity of burrow walls respect to that in undisturbed soils [71–73]. Dissipation of APIs in earthworms’ biostructures (burrow walls, casts and middens) needs
to be further explored to know the impact of both anecic and endogeic earthworms in
the environmental fate of APIs in agricultural soils. Recently, Briones and ÁlvarezOtero [74] reported marked differences in the cuticle and epidermis thickness of the
three ecological groups of earthworms. Anecic species have thickest cuticle
(4.03 Æ 1.6–5.72 Æ 1.7 μm, range of mean Æ SD) and epidermis
(42.7 Æ 16.7–46.3 Æ 9.7 μm) than epigeic (cuticle ¼ 1.51 Æ 0.4–3.21 Æ 1.5 μm,
epidermis ¼ 24.7 Æ 5.2–39.4 Æ 14.5 μm) and endogeic species
(cuticle ¼ 0.46 Æ 0.15–1.22 Æ 0.52 μm, epidermis ¼ 31.1 Æ 7.5–38.9 Æ 10.5 μm).
Beside the taxonomical and ecological meaning, these species-specific differences in
the tegument thickness may be relevant in ecotoxicology. Past studies using
E. andrei as model already demonstrated that the uptake of organochlorine pollutants takes place across the skin and the gastrointestinal epithelium [75]. Using a
three-compartment model (soil-earthworm tissue-gut content), the researchers found
that the uptake of organochlorine compounds via gastrointestinal tract was a significant bioaccumulation route for highly hydrophobic chemicals (log K OW > 6)
[75]. In addition, the transfer across the skin decreased as the K OW value of the
organochlorine compounds increased. Probably, the mucous secretion of skin and
the cuticle layer contributed to reduce the uptake of highly hydrophobic pollutants
through the skin. The role of the cuticle thickness in API bioaccumulation may be
supported by the data in the study by Carter et al. [76]. These researchers compared
the bioconcentration factors and uptake rates of four APIs (carbamazepine,
Vermiremediation of Pharmaceutical-Contaminated Soils and Organic Amendments
347