this suggests that earthworm uptake is a complex interaction of a variety of factors
and processes and does not exclusively rely on a single soil parameter.
Research to date has primarily been carried out using the model species in soil
ecotoxicology, Eisenia fetida, which is a suggested test species in TGD guidelines.
Whilst this is not a native soil-dwelling species, preferring to instead occupy high
organic content manures, it is easy to maintain in laboratory cultures. However,
biological attributes such as species size, feeding habits and reproduction have been
widely reported to play a key role in the uptake and bioconcentration of a range of
chemicals including metals and DDE [109–111]. Differences in the uptake of
pharmaceuticals between E. fetida and the larger deep-burrowing earthworm,
Lumbricus terrestris, have also been observed [112]. In a single soil type, BCFs
for carbamazepine and diclofenac were similar between species, whereas for fluoxetine and orlistat, BCFs in E. fetida were more than double those seen in L. terrestris.
Differences in rates of accumulation between species were also observed, with
uptake rates faster in E. fetida, with the exception of carbamazepine. Observed
differences between species such as this raise concerns around the use of a single
test organism in risk assessments and bring into question if the current selected
species, E. fetida, is representative of the diverse array of earthworm species that
co-exist in the soil environment.
Given that earthworms occupy a low trophic level in terrestrial food webs, uptake
and accumulation of pharmaceuticals by earthworms might serve as the entry point
for these chemicals into terrestrial food webs and a route of exposure for higher
trophic organisms. To date, wildlife exposure to pharmaceuticals remains poorly
characterised with only a handful of published studies on this topic. Whitlock et al.
[113] detected residues of the antidepressant fluoxetine in wild-grown Eurasian
starlings (Sturnus vulgaris) feathers at concentrations up to 27.0 ng/g, providing
some first evidence of pharmaceutical exposure in the wild. Nevertheless, accumulation of pharmaceuticals in the food chain has the potential to result in secondary
toxicity. For example, [114] observed effects in S. vulgaris movement after ingestion
of wax worms contaminated with fluoxetine and exposure to xenobiotic estrogenic
compounds at concentrations similar to that observed in earthworms collected from
trickling filter beds resulted in significant enlargement of the high vocal centre
(portion of the brain controlling song production), increased song production and
complexity and a decrease in immune function in S. vulgaris [115, 116].
Nevertheless, the BCFs calculated in laboratory exposures as well as calculated
from earthworms sampled from the field are all relatively small (<100) and would
suggest the potential for food chain transfer and secondary toxicity is minimal.
However, more research is clearly needed to investigate a wider suite of pharmaceuticals, in a broader range of soil types to fully assess the environmental risk of
earthworm exposure to these bioactive chemicals. In addition, whilst we know very
little about the uptake of pharmaceuticals by earthworms, we know even less about
the accumulation of pharmaceuticals by other soil organisms (e.g. springtails and
enchytraeids), which also occupy the soil environment and present a risk via food
chain transfer.
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L. J. Carter et al.
and processes and does not exclusively rely on a single soil parameter.
Research to date has primarily been carried out using the model species in soil
ecotoxicology, Eisenia fetida, which is a suggested test species in TGD guidelines.
Whilst this is not a native soil-dwelling species, preferring to instead occupy high
organic content manures, it is easy to maintain in laboratory cultures. However,
biological attributes such as species size, feeding habits and reproduction have been
widely reported to play a key role in the uptake and bioconcentration of a range of
chemicals including metals and DDE [109–111]. Differences in the uptake of
pharmaceuticals between E. fetida and the larger deep-burrowing earthworm,
Lumbricus terrestris, have also been observed [112]. In a single soil type, BCFs
for carbamazepine and diclofenac were similar between species, whereas for fluoxetine and orlistat, BCFs in E. fetida were more than double those seen in L. terrestris.
Differences in rates of accumulation between species were also observed, with
uptake rates faster in E. fetida, with the exception of carbamazepine. Observed
differences between species such as this raise concerns around the use of a single
test organism in risk assessments and bring into question if the current selected
species, E. fetida, is representative of the diverse array of earthworm species that
co-exist in the soil environment.
Given that earthworms occupy a low trophic level in terrestrial food webs, uptake
and accumulation of pharmaceuticals by earthworms might serve as the entry point
for these chemicals into terrestrial food webs and a route of exposure for higher
trophic organisms. To date, wildlife exposure to pharmaceuticals remains poorly
characterised with only a handful of published studies on this topic. Whitlock et al.
[113] detected residues of the antidepressant fluoxetine in wild-grown Eurasian
starlings (Sturnus vulgaris) feathers at concentrations up to 27.0 ng/g, providing
some first evidence of pharmaceutical exposure in the wild. Nevertheless, accumulation of pharmaceuticals in the food chain has the potential to result in secondary
toxicity. For example, [114] observed effects in S. vulgaris movement after ingestion
of wax worms contaminated with fluoxetine and exposure to xenobiotic estrogenic
compounds at concentrations similar to that observed in earthworms collected from
trickling filter beds resulted in significant enlargement of the high vocal centre
(portion of the brain controlling song production), increased song production and
complexity and a decrease in immune function in S. vulgaris [115, 116].
Nevertheless, the BCFs calculated in laboratory exposures as well as calculated
from earthworms sampled from the field are all relatively small (<100) and would
suggest the potential for food chain transfer and secondary toxicity is minimal.
However, more research is clearly needed to investigate a wider suite of pharmaceuticals, in a broader range of soil types to fully assess the environmental risk of
earthworm exposure to these bioactive chemicals. In addition, whilst we know very
little about the uptake of pharmaceuticals by earthworms, we know even less about
the accumulation of pharmaceuticals by other soil organisms (e.g. springtails and
enchytraeids), which also occupy the soil environment and present a risk via food
chain transfer.
204
L. J. Carter et al.