Forest type effects on the retention of radiocesium in organic layers of forest ecosystems affected by the Fukushima nuclear accident

The Fukushima Daiichi nuclear power plant disaster caused serious radiocesium (137Cs) contamination of forest ecosystems over a wide area. Forest-floor organic layers play a key role in

controlling the overall bioavailability of 137Cs in forest ecosystems; however, there is still an insufficient understanding of how forest types influence the retention capability of 137Cs

in organic layers in Japanese forest ecosystems. Here we conducted plot-scale investigations on the retention of 137Cs in organic layers at two contrasting forest sites in Fukushima. In a

deciduous broad-leaved forest, approximately 80% of the deposited 137Cs migrated to mineral soil located below the organic layers within two years after the accident, with an ecological

half-life of approximately one year. Conversely, in an evergreen coniferous forest, more than half of the deposited 137Cs remained in the organic layers, with an ecological half-life of 2.1

years. The observed retention behavior can be well explained by the tree phenology and accumulation of 137Cs associated with litter materials with different degrees of degradation in the

organic layers. Spatial and temporal patterns of gamma-ray dose rates depended on the retention capability. Our results demonstrate that enhanced radiation risks last longer in evergreen

coniferous forests than in deciduous broad-leaved forests.

As a result of the accident at the Fukushima Daiichi nuclear power plant (NPP) in March 2011, more than several tens of thousands of hectares of forests in Japan experienced severe

radioactive contamination1. Of the radionuclides found in the atmospheric fallout from the accident, radiocesium (137Cs), with a half-life of 30.1 years, is the primary source of concern,

because over the coming decades, forest ecosystems contaminated with 137Cs will enhance the radiation exposure of the local population via both the elevated ambient air dose rate (external

exposure) and the consumption of contaminated forest products (internal exposure)2.

One of the most important lessons learned from observational studies of 137Cs migration in European forests after the Chernobyl NPP accident was that forest-floor organic layers retain the

largest portion of the fallout 137Cs for a long time (over a decade) because they are a prolonged source for 137Cs recycling (i.e., the uptake of 137Cs by trees from the organic layers and

the subsequent redeposition of 137Cs onto the forest floor via litterfall) in forest ecosystems3,4,5,6,7. This is primarily because organic layers are deficient in clay minerals that offer

specific sites for 137Cs adsorption8,9, and therefore, 137Cs in these layers is not strongly fixed and remains potentially mobile and bioavailable7,10. However, it is well documented that

once 137Cs is transferred to the mineral soil located below the organic layers, it is rapidly immobilized in the upper layers of the mineral soil via its interactions with clay

minerals11,12. The fixation of 137Cs by clay minerals in the mineral soil results in a reduced availability for 137Cs uptake by plant roots4,13,14. The striking contrasts in the mobility and

bioavailability of 137Cs between the organic and mineral soil layers suggests that the retention of 137Cs in organic layers is a key factor in evaluating radiation risks delivered from

137Cs contamination of forest ecosystems.

Deciduous broad-leaved forests (49.1% of the forested area) and evergreen coniferous forests (47.0%) are the dominant forest types in the area heavily affected by the Fukushima NPP accident

in Japan1. These forests greatly differ in their tree phenology, which is one of the most important drivers of ecosystem processes, and therefore, it is very likely that the behavior of

137Cs in the forest ecosystems after atmospheric fallout differs depending on the forest type. The tree canopies of evergreen coniferous forests acted as efficient filters of the atmospheric

plume of 137Cs from the Fukushima NPP accident; therefore, a large proportion of 137Cs was initially intercepted and retained by the tree canopies and subsequently transferred to the forest

floor via processes such as throughfall, stemflow, and litterfall15,16. By contrast, the canopy-interception effect was less important in deciduous broad-leaved forests compared to

evergreen coniferous forests because the deciduous forests were leafless at the time of the accident; therefore, a large proportion of 137Cs delivered by the Fukushima NPP accident was

directly deposited on the forest floor16,17,18. Therefore, it is easily assumed that the differences in 137Cs deposition behavior between the forests will result in different capacities of

137Cs retention in their organic layers, at least over the first several years following forest contamination.

The rate of decomposition of litter materials in organic layers and the subsequent release of bioavailable 137Cs are also important factors in controlling the rate of 137Cs recycling within

a forest ecosystem, and these factors are largely dependent on the forest type. Deciduous leaf fall is an annual occurrence and the decomposition of broad leaves in such forests has been

shown to be rapid19,20, whereas the mean leaf longevity of evergreen coniferous trees is longer than a year21 and the decomposition of needle-like leaves appears to be much slower compared

to broad leaves22,23. The rate of decomposition of litter materials in organic layers is also influenced by climatological factors such as temperature and precipitation. Therefore, it is

suggested that the behavior of 137Cs in organic layers differs between European forests (affected by the Chernobyl NPP accident) and Japanese forests (affected by the Fukushima NPP

accident)24,25,26; studies under specific climatological and ecological conditions in Japan are urgently required to assess the environmental consequences of the Fukushima NPP accident. In

addition, forests have complex stand structures and microtopography, and therefore, the quantity and quality (degrees of degradation) of litter materials accumulated in organic layers are

highly spatially variable, even within a forest ecosystem27. Spatial heterogeneity can also be a complicating factor in quantitatively assessing the retention capability of organic layers

for 137Cs and its dependence on the forest type20,28.

Therefore, even though forest-floor organic layers are of key importance in 137Cs cycling in forest ecosystems, there is still an insufficient understanding of how much and for how long

organic layers can retain 137Cs in Japanese forest ecosystems affected by the Fukushima NPP accident. To explore the role of organic layers in 137Cs retention, we conducted plot-scale

investigations at two contrasting forest sites in Fukushima, Japan (Fig. 1). We collected samples from the organic and underlying mineral soil (0–5 cm) layers at 25 locations within each of

the 20 m × 20 m plot areas established in the deciduous broad-leaved forest (DBF) and evergreen coniferous (Japanese cedar-dominated) forest (CF). Litter samples in organic layers were

collected separately from the upper L layer (litter layer, consisting of intact and relatively undecomposed leaves) and the lower F layer (fermentation layer, consisting of partially and

well-degraded plant residues). The sample collections were conducted in December 2012 (21 months after the Fukushima NPP accident) at the DBF site and in August 2013 (29 months after the

accident) at the CF site, and the collected samples were analyzed for radiocesium isotopes (137Cs and 134Cs) and for organic carbon (C) and total nitrogen (N). Based on the results, we

evaluated the forest type effects on, and plot-scale spatial variability in, the retention behavior of 137Cs in the organic layers of Japanese forest ecosystems to obtain insights into the

radioecological consequences of the Fukushima NPP accident.

(a) Location of the study site and photographs of (b) the DBF and (c) CF investigated in this study. The 137Cs inventory map was generated using the website “Extension Site of Distribution

Map of Radiation Dose, etc.” prepared by MEXT, Japan53. Photographs were taken at the time of sample collection by T. Matsunaga.

At both forest sites, 137Cs concentrations were higher in the organic layer (L and F layers) than in the topsoil (0–5 cm) layer (Table 1; also see Tables S1 and S2 in Supplementary

information). Within the organic layer, the concentrations showed a different depth-wise pattern between the sites; 137Cs was specifically concentrated in the lower F layer at the DBF site,

whereas 137Cs concentration was fairly similar between the L and F layers at the CF site.

The measured 137Cs and 134Cs concentrations showed a similar pattern of distribution for all samples. The 134Cs/137Cs activity ratios were 0.56 ± 0.03 and 0.46 ± 0.02 (mean ± standard

deviation) for the litter and soil samples collected at the DBF and CF sites, respectively (Table 1). The ratios were close to those (0.57 and 0.46, respectively) theoretically predicted for

Fukushima-derived radiocesium at the time of sample collection, the initial ratio being unity in March 2011 and decreasing according to different rates of radioactive decay (the physical

half-lives of 137Cs and 134Cs are 30.1 and 2.1 years, respectively). The ratios indicate that the radiocesium isotopes observed in the present study originate from the Fukushima NPP

accident. For simplicity, we will discuss only 137Cs results in the following parts of this paper.

The total inventories of 137Cs in the forest surface soils (organic and topsoil layers) were 49.8 ± 11.0 kBq m−2 (mean ± standard deviation, n = 25) at the DBF site and 43.8 ± 12.1 kBq m−2

(n = 25) at the CF site (Table 1), and showed spatially heterogeneous distributions within the 20 m × 20 m plot areas (Figs 2b and 3b). The difference in the total 137Cs inventory between

the sites was not considered to be statistically significant (P = 0.07 via the unpaired t-test). Coefficients of variation (CV) values of the total 137Cs inventory, calculated as the ratio

of the standard deviation to the mean (i.e., relative standard deviation), were 22.1% and 27.5% for the DBF and CF sites, respectively. In both plots, the spatial distribution of the total

137Cs inventory was not found to be related to that of the standing trees (Figs 2 and 3). There was no statistically significant (at a 5% significance level) correlation between the total

137Cs inventory and the stand basal area in the 4 m × 4 m subplot (calculated as the sum of the cross-sectional areas at breast height for all trees in the target subplot) (Table 2).

Spatial distribution maps of (a) the sampling points and standing trees, (b) the total 137Cs inventory in the organic and topsoil layers, (c) the 137Cs inventory in the organic layer, and

(d) the gamma-ray dose rate at the ground surface in the 20 m × 20 m plot area of the DBF. In (a), open squares indicate the sampling points, filled circles indicate the standing trees

(represented by their breast height diameters), filled diamonds indicate the stones (larger than 10 cm in diameter), open circles indicate the hollows in the land, and the filled rectangle

indicates the area covered by a vinyl sheet.

Spatial distribution maps of (a) the sampling points and standing trees, (b) the total 137Cs inventory in the organic and topsoil layers, (c) the 137Cs inventory in the organic layer, and

(d) the gamma-ray dose rate at the ground surface in the 20 m × 20 m plot area of the CF. In (a), open squares indicate the sampling points and filled circles indicate the standing trees

(represented by their breast height diameters).

Although the total 137Cs inventories in the surface soils at the two sites were similar, the inventories in the organic (L + F) layers were quite different. The inventories of 137Cs in the

organic layers were 10.0 ± 3.2 kBq m−2 (CV: 31.9%) and 23.0 ± 5.5 kBq m−2 (CV: 24.1%) at the DBF and CF sites, respectively (Table 1). At the DBF site, a large proportion (78.8 ± 8.4%) of

the total 137Cs inventory was found in the topsoil layer below the organic layer. By contrast, at the CF site, more than half (54.0 ± 12.2%) of the total inventory still remained in the

organic layer, even though the sample collection at this site was conducted approximately 8 months after the sample collection at the DBF site.

The 137Cs inventory in organic layers has been investigated several times at these sites since the accident in March 201129,30. This allows us to assess the temporal changes in the 137Cs

inventory in the layers during the first three-year period (Fig. 4). The 137Cs inventory in the organic layers decreased with time at both sites and this decreasing pattern can be

characterized by an exponential decay model:

Temporal changes in the 137Cs inventory in the organic (L + F) layers of the two contrasting forests since the Fukushima NPP accident.

The data are decay-corrected to the sampling date. Previous studies were conducted in June 201129, July 201130, and March 2012 (Koarashi et al., unpublished).

where It is the 137Cs inventory (kBq m−2) in the organic layer at time t, I0 is the 137Cs inventory (kBq m−2) in the layer at time t = 0, λ is the decay constant (y−1), and t is the elapsed

time (y) since the accident. The effective half-life (Teff in years) of 137Cs in the organic layer can, therefore, be calculated as Teff = ln(2)/λ. Because the 137Cs inventory data presented

in Fig. 4 are decay-corrected to the sampling date, the effective half-life is a measure of the combined effect of physical (radioactive) decay and ecological elimination processes. The

ecological half-life (Te in years) of 137Cs in the organic layer can, therefore, be evaluated as

where Tp is the physical half-life of 137Cs (30.1 years). The ecological half-lives of 137Cs estimated in this way were 0.95 years (r = 0.90) and 2.1 years (r = 0.98) for the organic layers

at the DBF and CF sites, respectively.

The spatial distribution of the 137Cs inventory in the organic layer showed a similar pattern to that of the total 137Cs inventory at the CF site (Fig. 3), and there was a significant

positive (r = 0.49, p