7. General Framework
7.10. Linking Exposure and effects
7.10.2. Exposure routes of key drivers
In-soil organisms are exposed to PPPs via a variety of pathways. This is modulated mainly by their morphology (e.g. their body form or the structure of the epidermis), physiology (e.g. the way they take up water, food and oxygen) and behaviour (where they live and move in soil) (Peijnenburg et al., 2012). Moreover, these pathways may vary during the life cycles of some species. The relative relevance of these uptake routes for the body burdens is also dependent on the properties of the chemical (e.g. hydrophobicity) and environmental conditions like soil properties and climate.
The major uptake routes considered for soil organism are:
•
Contact with soil, soil pore water and litter (so diffusion into the body via the ‘skin’);•
Ingestion of food (soil organic matter, litter, bacteria, fungi, prey), of soil particles and soil water;A usual distinction is made between the so called ‘soft-bodied’ and the ‘hard-bodied’ organisms.
The former include earthworms, enchytraeids, nematodes, some collembola and insect larvae, whereas the latter are composed by collembolans living in the upper soil profile, mites, insects and the epigeic detritivores– isopods and millipedes – and predators like spiders and centipedes.
For ‘soft-bodied’ organisms, where water and oxygen is taken up mainly via the skin, soil pore-water is considered the most important uptake route for chemicals (Belfroid et al., 1994; EFSA, 2009c;
De Silva et al., 2010; Smıdova and Hofman, 2014; Diez-Ortiz et al., 2015). Ingestion of contaminated food and soil particles and the subsequent absorption of chemicals via the gastrointestinal tract, however, can play a significant role as well (Smıdova and Hofman, 2014; Katagi and Ose, 2015).
According to Belfroid et al. (1995), laboratory studies performed with earthworms and a range of PPPs showed that the uptake deviates by a factor lower than two when compared by model predictions based on equilibrium partitioning theory (EPT). However, differences between species with different life-forms should be taken into account. Belfroid et al. (1994) found higher accumulation factors for Eisenia andrei (an epigeic species feeding mainly on humic material) than for Lumbricus terrestris (an anecic species feeding mainly on plant litter), which could indicate that uptake via soil could be of less importance for anecic species. On the other hand, anecics do ingest large amounts of soil when burrowing and looking for food, and evidence of temporary increase in internal concentration of hexachlorobenzene (HCB) was found in Lumbricus terrestris when placed in a new contaminated soil and after the creation of new burrows (Beyer, 1996). Jager et al. (2003) and Katagi and Ose (2015) present two-compartment models for earthworms, including the adsorption of contaminants from the food via the gut. Jager et al. (2003) points to the fact that the contribution of the gut route increased Figure 15: Schematic representation of the two types of exposure assessments that are needed in
any combination of tiers of the effect andfield-exposure flowcharts
with increasing hydrophobicity of the chemical. For the tested substance with highest Kow values, the gut route clearly dominated. Moreover, measured concentrations in the worms exceed equilibrium with the soil and bioconcentration increased more with higher Kow than did soil sorption. Interestingly, the rate constant for exchange across the skin in the soil environment is much higher for hydrophobic compounds than an exchange in a‘water-only’ situation would predict.
‘Hard-bodied’ organisms take up water and oxygen via special organs. For these organisms, ingestion of food is also a relevant exposure pathway. However, as expected, assimilation rates of the different food items play a key role in modulating the actual uptake in the digestive tract, and unfortunately not many studies exist on this topic, especially when dealing with microbivores (mainly collembolan and mites that are fungal and bacterial feeders) and predators (especially predatory mites). ‘Hard-bodied’ organisms can also take up chemicals via contact with soil and/or soil pore water, as demonstrated for collembolans (Gyldenkaerne and Jorgensen, 2000; Fountain and Hopkin, 2005;
EFSA, 2009c) and isopods (e.g. Sousa et al., 2000; Santos et al., 2003). The former authors found that uptake from soil pore water was the major route for pyrethroids and dimethoate. Regarding isopods, Sousa et al. (2000) reported that internal concentrations of lindane in Porcellionides pruinosus exposed via soil were 25 times higher than when exposed through food, which were due to different degradation kinetics of the active substance in the two matrices. Santos et al. (2003) found that internal body burdens in the same species and also for lindane were better correlated with Figure 16: Scientific concepts on the bioavailability of organic chemicals. (Reprinted with permission from Ortega-Calvo J, Harmsen J, Parsons J, Semple K, Versonnen B, Aitken M, Ajao C, Eadsforth C, Galay-Burgos M, Naidu R, Oliver R, Peijnenburg W, Roembke J and Streck G, 2015. From bioavailability science to regulation of organicbchemicals. Environmental Science and Technology, 49, 10255–10264. Copyright (2015) American Chemical Society).
Bioavailability can be examined through chemical activity, the potential of the contaminant for direct transport and interaction with the cell membrane (processes B, C and D), or bioaccessibility measurements, which incorporate the time-dependent phase exchange of the contaminant between the soil/sediment and the water phase (process A). Depending on biological complexity, the passage of the contaminant molecule across the cell membrane (process D) may represent multiple stages within a given organism before the site of biological response is reached (process E)
concentration in soil extracts than in bulk soil. Similar findings were also reported by Belfroid and Van gestel (1999) for soft-bodied organisms like slugs, where accumulation of DDT via soil was 10-fold higher than via food. Nevertheless, uptake via feeding on the litter layer should not be excluded as an important exposure pathway, especially for very hydrophobic compounds (Van Brummelen et al., 1996). Furthermore, exposure in the litter layer does not occur only via feeding but also via contact with the litter and its water-film. The results mentioned above are based on laboratory studies and generalisations to a real field scenario should be made carefully, as should generalisations to other species, even within the same group of organisms, due to the low number of species tested.
Taking a pragmatic approach in terms of conducting a risk assessment, a major uptake route for
‘soft-bodied’ organisms (e.g. earthworms, enchytraeids, soft bodied collembola, nematodes and some insect larvae) seems to be the uptake from soil pore water. Moreover, the concentration in pore water is also considered to be the driving factor for uptake and toxicity of pesticides for microorganisms.
However, the relative importance of other uptake routes depends on the properties of the assessed active substance and will increase with increasing hydrophobicity of the chemical.
Regarding‘hard-bodied’ organisms (e.g. some collembolans, mites, isopods), although contact with soil plays a role, evidences of the importance of soil pore water as an important exposure route to these organisms does also exist. This stresses the importance of considering exposure of in-soil organisms to pore water as well, particularly for compounds that have high water solubility. The Scientific Opinion on the effect assessment for pesticides on sediment organisms in edge-of-field surface waters (EFSA PPR Panel, 2015b) states that the freely dissolved fraction in pore-water of sediment-associated PPPs most likely is the main exposure route for these organisms, although dietary exposure might also play a role.
Regarding uptake via food, namely for those organisms feeding on fungi, bacteria, soil organic matter, and for predatory organisms, not many data are available and the derivation of robust concentrations in these matrices is, for the moment, a difficult task. Furthermore, evidence exists that this uptake route has high relative relevance for compounds with a high Kow.
Particular attention should be given to the litter layer (EFSA PPR Panel, 2010c). Even if the definition of a‘proper’ litter layer includes certain stability over time, dead organic matter as plant debris is located on the soil surface of most crop systems during the vegetation period and after harvest. Plant debris constitutes an important food source for anecic earthworms, like L. terrestris, and litter dwelling organisms also in non-permanent crops, with consequent relevance as an uptake pathway for active substances, and there is also potential uptake via contact with the litter material. This would be more common in annual crops with low or no tillage and permanent crops. Exposure from the litter should therefore, be taken into consideration, whether from a litter layer or from plant debris on the soil surface.
Table 21: Exposure routes of key drivers belonging to the in-soil organisms
Group affected Exposure route
Litter layer/waterfilm Fragmented litter, fungi
& bacteria Decomposers Microorganisms (fungi, bacteria) Litter layer/waterfilm (fragmented) litter Soil dweller
Soil and soil pore water Dead organic matter, fungi & bacteria