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Environmental fate & pathways

Bioaccumulation: terrestrial

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Description of key information

The biota-to-soil accumulation factor (BSAF) for earthworms in soil is dependent on the effective cation exchange capacity (eCEC) of the soil:

log BSAF (kgdw/kgdw) = -0.89 * log eCEC (cmolc/kg) +0.55

For comparison with the PNECoral for birds and mammals, this BSAF must be expressed on a fresh weight basis. The conversion of dry weight to fresh weight is based on an average dry matter of 16% in earthworms (Jager 1998):

BSAF (kgdw/kgdw) = 0.16 * BSAF (kgdw/kgdw)

A generic BSAF factor of 0.048 (fresh weight) is derived for a soil with a median eCEC of 16 cmolc/kg soil. Fresh-weight based BSAF values for a soil with an eCEC of 8 and 30 cmolc/kg soil, corresponding to the 10thand 90thpercentile of eCEC in European arable soils are 0.089 and 0.028, respectively.

Key value for chemical safety assessment

Additional information

A wealth of data is available on biota-to-soil accumulation factors (BSAF) for Pb. A literature search has been performed in 2017 to assess the published BSAF. Data were considered reliable:

  1. if the data came from field studies or laboratory studies using soil and biota collected at the same field site. This is to ensure that biota Pb burdens are in equilibrium with soil Pb concentrations. Data from laboratory studies where Pb was added to the soil as a Pb salt are excluded;
  2. if Pb concentrations were measured in soil and biota. The Pb concentration in soil has to be expressed as “total” soil Pb (e.g. Pb measured afteraqua regiadestruction), extractable Pb fractions (e.g. water-extractable Pb) are not considered reliable;
  3. if guts from the biota were voided prior to analysis;
  4. if it was indicated how BSAF values were expressed, i.e. on a dry or wet weight basis.

According to the REACH Guidance Document (Chapter R16), the food-chain soil, earthworms and earthworm eating predators is considered for risk characterisation purposes.

In total, 248 BSAF values for earthworms were identified that meet the reliability criteria, ranging from 0.01 to 22.05 kgdw/kgdw. The median BSAF for earthworms on a dry weight basis is 0.23 kgdw/kgdw(10-90thpercentiles are 0.06-1.19).

Results are available for several earthworm species, belonging to different ecological groups of earthworms: anecic, endogeic and epigeic earthworms. No distinct differences in BSAF values across these groups could be identified. Moreover, different species were sampled in different soils, which hampers a sound comparison of the data.

  • Anecic earthworms (n=46):                      range: 0.06-1.76, median: 0.41
  • Endogeic earthworms (n=108):                range: 0.01-22.05, median: 0.18
  • Epigeic earthworms (n=61):                     range: 0.02-9.15, median: 0.17
  • mixed or not reported (n=33)                    range: 0.06-1.25, median: 0.25

Soil properties were not reported for all BSAF values, but based on the reported data, it can be concluded that the BSAF values are derived in a wide range of soils and the data available can be considered as representative for soils in Europe:

  • pH:                                                3.0 – 8.4                             (n=217)
  • Organic carbon content                 1.1 – 24.6 %                       (n=186)
  • Clay content                                  4 – 53 %                             (n=111)
  • Cation exchange capacity              5.3 – 78.8 cmolc/kg         (n=114)
  • Total Pb content in soil                  9.4 – 16700 mg/kg           (n=231)

Only CEC is significantly correlated with BSAF values. No significant correlation with Pb content, pH, Organic carbon content or clay content is observed. Because of the lack of any effect of Pb level in soil on the BSAF for Pb in earthworms, also data from Pb contaminated soils were included in the analysis.

Four field studies reported CEC data for the soils where earthworms have been sampled (Ma, 1982, Beyer et al., 1982, Ernst et al., 2008 and Nannoni et al., 2011). Correlations between BSAF and soil properties for individual studies are either non-significant or contradictory. The combined dataset shows a significant decrease of BSAF values with increasing eCEC (effective CEC) of the soil:

Log BSAF = -0.89 * log eCEC +0.55            R2= 0.16, P<0,01                                                   (1)

The R2of this correlation is low, but the correlation is highly significant and one must notice that this regression is based on data from different studies, for 9 different earthworm species (anecic: Aporrectodea longa, Lumbricus terrestris; endogeic: Aporrectodea caliginosa, Aporrectodea rosea, Aporrectodea tuberculate, Octolasion cyaneum, Octolasion tyrtaeum; epigeic: Lumbricus rubellus, Dendrodrilus rubidus) and for a wide range of Pb levels and forms in soil (from natural and various anthropogenic sources). No clear distinction could be noticed between different ecological groups of earthworms.

In a recent laboratory study on the effects of soil type on the bioavailability and toxicity of lead salts to earthworms, the internal body concentrations and bioaccumulation factors for Pb were measured for Eisenia fetida exposed for 28 days to Pb in 6 different soils spiked with PbCl2(Lanno, 2012 and 2015,Table1). Bioaccumulation factors were determined forthe 2 test concentrations bracketing the EC10for reproduction of E. fetida in these soils.

Table1: Bioaccumulation factors for Eisenia fetida in different soils (expressed on a dry weight basis: kg dw/kg dw, each value is the average of 6 observations: 3 replicates for each of 2 test concentrations).

Soil

Country

Land use

pH*

Total Pb (mg/kg)

Organic carbon (%)

Clay
(%)

eCEC*
(cmolc/kg)

EC10*

(mg/kg)

BSAF

Barcelona

Spain

arable land

7.4

135

1.2

16

14.3

468

0.050

Woburn

UK

grassland

6.1

46

4.3

30

26.5

362

0.035

De Meern

The Netherlands

grassland

5.3

52

5.0

60

42.0

1375

0.075

Borris

Denmark

arable land

5.7

15

1.5

3

4.2

64

0.655

Hygum

Denmark

grassland

5.2

18

2.1

13

7.6

95

0.365

Kasterlee

Belgium

arable land

4.7

24

2.3

2

4.0

29

0.248

pH in 0.01M CaCl2; eCEC= effective cation exchange capacity, i.e. CEC at pH of the soil; EC10 for reproduction of E. fetida.

The best regression between BSAF and soil properties for the dataset of Lanno (2015) was also found to be a linear regression of log-transformed BSAF values and log-transformed eCEC of the soils:

Log BSAF = -1.02 * log eCEC +0.23            R2= 0.70, P<0,05                                                   (2)

Comparison of the regression based on the compiled field data (equation 1) and this regression for E. fetida exposed to Pb in soil under laboratory conditions (equation 2) yields the following observations:

  • The slopes are similar, illustrating a similar effect of CEC on Pb accumulation in earthworms.
  • The R2value of 0.70 for the effect of CEC in the study with one species and under controlled exposure conditions is much higher than the R2of 0.16 for the field data. It is concluded that also in the field, CEC has a significant effect on bioavailability of Pb to earthworms, but that this effect is partly obscured by the variation in forms of Pb, earthworm species etc.
  • The intercept of the regressions based on the laboratory exposure of E. fetida (equation 2) is a factor 2 smaller than the corresponding regression after field exposure (equation 1), suggesting a difference in the absolute value of the BSAF depending on the exposure conditions or earthworm species tested. This observation confirms the choice only to select BSAF data from field studies or laboratory studies using soil and biota collected at the same field site to ensure that biota Pb burdens are in equilibrium with soil Pb concentrations.

The significant regression between log BSAF and log CEC is also consistent with the regression observed between toxicity of Pb toE. fetidareproduction and eCEC of the soil (see section 7.2 of the CSR).

Because of the significant effect of CEC of the soil on bioavailability and uptake of Pb by earthworms and because the relevance of the median BSAF value of 0.22 (dry weight basis) is not clear (unknown bias towards soils with high or low bioavailability as CEC is not reported for 134 out of 248 observations), it is concluded to implement the effect of soil properties by using the overall regression between log CEC and log BSAF (equation 1).

This yields a generic BSAF of 0.30 (dry weight basis) for the median eCEC value of 16 cmolc/kg soil for European natural soils (GEMAS, Geochemical Mapping of Agricultural and Grazing Land Soils;http://gemas.geolba.ac.at/; Reimann et al., 2014).

The conversion of dry weight to fresh weight is based on an average dry matter of 16% in earthworms (default value in EUSES, Jager 1998).

This yields a generic fresh-weight based BSAF of 0.048 for a soil with a median eCEC of 16 cmolc/kg soil and BSAF values of 0.089 and 0.028 for a soil with an eCEC of 8 and 30 cmolc/kg soil, respectively, corresponding to the 10thand 90thpercentile of eCEC in European arable soils.

 

A few literature data are available for bioaccumulation of Pb in isopods from soil or litter, 14 BSAFs were collected. Values range from 0.001-0.65 kgdw/kgdw. A median BSAF for isopods on a dry weight basis is 0.04 (median of 14 values).

Table: Bioaccumulation factors between soil or decomposed leaf litter and isopods. The Pb concentrations in the biota are the product of BAF and soil Pb concentration.

Test substance

Organism

Test conditions

Medium

Duration

Soil/litter (mg Pb/kgdw)

BAF (kgdw/kgdw)

Reference

Pb-soil

Porcellio scaber

15 adult specimen were exposed for 14 days to approximately 600 mL of air-dried experimental soil (polluted and remediated with 2.5, 10, 40 and 4 x 40 EDTA, respectively) in plastic vessels with plastic covers.

polluted soil

14 days

4603

0.04

Udovic et al. 2009

polluted soil leached with 2.5 mmol kg-1EDTA

4323

0.04

polluted soil leached with 10 mmol kg-1EDTA

2712

0.035

polluted soil leached with 40 mmol kg-1EDTA

2112

0.035

polluted soil leached with 4 x 40 mmol kg-1EDTA

1239

0.025

PbCl2

Porcellio scaber

Isopods were kept in plastic boxes on a moist gypsum base covered by decomposed leaf litter material, i.e. partly decomposed leaf litter material soaked in an aqueous solution of 100, 500 or 1000 mg l–1 Pb2+(as PbCl2).

Control

21 days

 

7.1

0.41

Gräff et al. 1997

100 mg Pb/l

517

0.14

500 mg Pb/l

2777

0.08

1000 mg Pb/l

7676

0.03

Pb-soil

Trachelipus rathkei

Near a smelting complex a transect of 5 soil sampling sites was taken

0.3 km from the smelting complex

whole life

61946

0.006

Rabitsch 1995

Porcellio scaber

0.3 km from the smelting complex

61946

0.002

Trachelipus ratzeburgi

0.5 km from the smelting complex on the other side of the low hill

1190

0.649

1 km from the smelting complex

4618

0.248

2.5 km from the smelting complex

516

0.322