2016-2-4

Decline in intertidal biota following the 2011 Great East Japan Earthquake and Tsunami and the accident at the Fukushima Daiichi Nuclear Power Plant: field observations

(Scientific Reports)


February 4, 2016
Toshihiro HORIGUCHI, Hiroaki SHIRAISHI
Center for Environmental Risk Research
National Institute for Environmental Studies

   The National Institute for Environmental Studies (NIES) has conducted field surveys in the intertidal zones of eastern Japan to investigate the ecological effects of the serious accident at the Fukushima Daiichi Nuclear Power Plant (FDNPP) that accompanied the 2011 Great East Japan Earthquake and Tsunami in March 2011. The first survey was conducted at 16 sites within a 20-km radius of FDNPP on December 14, 2011, in cooperation with the National Institute of Radiological Sciences and Fukushima Prefectural Government. The surveys have been continued since then.
   The number of intertidal species decreased significantly with decreasing distance from the power plant(P<0.001)、and no rock shell (Thais clavigera) specimens were collected near the plant, from Hirono to Futaba Beach (a distance of approximately 30 km) in 2012. The collection of rock shell specimens at many other sites hit by the tsunami suggests that the absence of rock shells around the plant in 2012 might have been caused by the nuclear accident in 2011.
   Quantitative surveys in 2013 showed that the number of species and population densities in the intertidal zones were much lower at sites near, or within several kilometers south of, the plant than at other sites (P<0.05) and lower than in 1995, especially in the case of Arthropoda (e.g., barnacles). There is no clear explanation for these findings, but it is evident that the intertidal biota around the power plant has been affected since the nuclear accident.
   This study was published in Scientific Reports on February 4, 2016.
(URL: www.nature.com/articles/srep20416)

1. Introduction

 Three nuclear reactors of the Fukushima Daiichi Nuclear Power Plant (FDNPP), belonging to the Tokyo Electric Power Company (TEPCO) went into meltdown after the powerful earthquake (M 9.0) and subsequent tsunami in eastern Japan in March 2011 (known as the “2011 Great East Japan Earthquake and Tsunami”). Hundreds of petabecquerels (PBq) of radionuclides were estimated to have been emitted from these reactors to the environment 1. It is important to recognize that the amount of radionuclides that leaked directly from the reactors into the sea was much more than that entering via fallout (The estimates by the Japan Agency for Marine-Earth Science and Technology for the amounts of radionuclides leaked from FDNPP reactors into the sea were as follows: direct leakage and fallout of 137Cs from March 21 to May 6, 2011 were estimated at 4.2–5.6 PBq and 1.2–1.5 PBq, respectively 2.). Even though the 1986 disaster at the Chernobyl Nuclear Power Plant in Ukraine had a much greater release of radionuclides (approximately 5300 PBq, excluding noble gases) 1, the Fukushima nuclear reactor accident could have more serious impacts on marine ecosystems because the Chernobyl Nuclear Power Plant was located inland.

 For comparison, the total amount of 137Cs emitted to the sea from the Windscale nuclear units (currently, the Sellafield Thermal Oxide Reprocessing Plants) along the west coast of northwestern England from 1952 to 1992 is considered to be 41 PBq, and the maximum annual emission of 137Cs was 5.2 PBq in 1975 3. The Fukushima nuclear disaster released almost the same amount of 137Cs as the maximum annual emission from the Sellafield plants (5.2 PBq) into the coastal waters of Fukushima over a relatively short period (from mid-March to early May 2011) 2, suggesting that the marine organisms around FDNPP, unlike those around Sellafield, might have experienced acute or sub-acute, rather than chronic, exposure to 137Cs and other radionuclides.

 To evaluate possible adverse effects on marine organisms close to FDNPP and in the surrounding area from harmful substances leaked from FDNPP into the sea (not only radionuclides but also other substances in the cooling water), we performed field surveys in the intertidal zones of eastern Japan, as 1) a preliminary field survey conducted at 16 sites within a 20-km radius of FDNPP on December 14, 2011 (9 months after the disaster), 2) detailed field surveys at 43 coastal sites in eastern Japan, not only in Fukushima but also in Chiba, Ibaraki, Miyagi and Iwate Prefectures, in April, July and August 2012, which were also hit by the tsunami on March 11, 2011, and 3) quantitative surveys of sessile organisms at seven sites representative of those used in the 2012 survey in May and June 2013.

2. Methods

Preliminary survey in 2011.

 A preliminary survey was conducted at 16 sites within a 20-km radius of FDNPP in Fukushima Prefecture, as the area impacted by high radionuclide concentrations and the tsunami, on December 14, 2011, nine months after the disaster, to visually observe the distribution of the rock shell Thais clavigera. The distributions of other intertidal biota, such as molluscs (bivalves, chitons, and herbivorous and carnivorous snails) and crustaceans (barnacles, crabs, hermit crabs and wharf roaches) were also observed.

Detailed surveys in 2012.

 In April, July and August 2012, detailed field surveys were conducted at 43 sites along the coast of eastern Japan, not only in Fukushima (as an area possibly receiving higher concentrations of radionuclides) but also in Chiba, Ibaraki, Miyagi and Iwate Prefectures (as areas possibly receiving lower or much lower concentrations of radionuclides), which were also hit by the tsunami on March 11, 2011. The surveys were conducted at 10 sites within a 20-km radius of FDNPP in Fukushima Prefecture on April 24 and 25, 2012. Similar surveys were conducted at 33 other sites in Chiba, Ibaraki, Fukushima, Miyagi and Iwate Prefectures in April, July and August 2012. The intertidal species observed were recorded, and all individuals of carnivorous snails, such as the rock shell (Thais clavigera) and the dog whelk (Nucella freycineti), were collected. The time needed for sample collection was also recorded to calculate the relative population density (i.e., the number of individuals collected per minute).

Quantitative surveys in 2013.

 Surveys of sessile organisms were conducted at seven sites in Ibaraki, Fukushima and Miyagi Prefectures in May and June 2013 using 50-cm × 50-cm quadrats. The sites were representative of those used in the 2012 surveys, in terms of substrate (i.e., tetrapods or similar concrete structures set along the coast for wave protection) as well as distance from FDNPP. Four sites—Tomioka fishing port, Okuma, Kubo-yaji and Urajiri—were located within a 20-km radius of FDNPP in Fukushima Prefecture. The other sites (Hasaki Beach in Ibaraki Prefecture; Kujihama Beach in Ibaraki Prefecture; and Ishinomaki in Miyagi Prefecture) were used as reference sites for comparison. Sessile organisms on the surface of tetrapods or similar concrete structures within a 50-cm × 50-cm quadrat were collected at 3 different elevations in the intertidal zone (lower, middle and upper intertidal zones) at each site. Specimens were preserved in 10% formaldehyde neutral buffer solution. After the species had been identified, the number of individuals and wet-weight were determined for each species at each sampling location and elevation at each survey site. Then we calculated population densities and species numbers in the intertidal zones.

Data analysis.

 We performed regression analysis to test if the number of species in the intertidal zones differed significantly with distance from FDNPP in the 2012 and 2013 surveys. To assess similarity in the biotic community structure of the intertidal zones in the 2013 survey, we conducted cluster analysis (group average method) on Bray-Curtis similarity matrices for the number of species, and for population density in terms of the number of individuals per square meter and whole wet-weight per square meter. Differences in the biotic community structure represented by Bray-Curtis similarity among site groups was tested by analysis of similarity (ANOSIM). Possible differences in population densities of Arthropoda (i.e., the number of individual per square meter) at sites around FDNPP (i.e., Tomioka fishing port, Okuma and Kubo-yaji) compared to those at other sites (i.e., Hasaki Beach, Kujihama Beach, Urajiri and Ishinomaki) were evaluated using a t-test under the assumption that they had approximately equal variances in the 2013 survey.

3. Results

Preliminary survey in 2011.

 Gastropods (herbivorous and carnivorous snails) and crustaceans (crabs, hermit crabs and wharf roaches) were absent at almost all sites, with the exception of a limited number of small barnacles, mussels and limpets. Among the 16 sites surveyed, only one individual rock shell, Thais clavigera, was collected, at Namikura in the town of Naraha.

Detailed surveys in 2012

 The number of intertidal species decreased significantly with decreasing distance from the power plant (regression analysis; P < 0.001) (Fig. 1).

 No rock shell (Thais clavigera) specimens were found at 8 of the 10 sites in Fukushima Prefecture within a radius of 20 km of FDNPP, surveyed on April 24 and 25, 2012, although specimens were collected at two sites north of FDNPP, namely Ukedo fishing port and Urajiri (Fig. 1). All of these sites were hit by the tsunami on March 11, 2011. Because there were also no rock shell specimens collected at Hirono, surveyed on April 10, 2012, the area without rock shells extended from Hirono to Futaba Beach, a distance of approximately 30 km (Fig. 1). These areas almost overlap within a 20-km radius of FDNPP but are slightly biased to the south (Fig. 1).

Figure 1. Numbers of intertidal species and the relative population densities of the rock shell (Thais clavigera) and dog whelk (Nucella freycineti) observed during surveys in 2012 along the coast of northeastern Japan.
Dotted circle indicates a radius of 20 km from the Fukushima Daiichi Nuclear Power Plant (FDNPP) in Fukushima Prefecture. Purple star marks the location of FDNPP. Red vertical bars on graphs and red dots on map indicate sites located within the 20-km radius of FDNPP.
*The partial map of Japan in this figure was modified by the authors from the map of Japan at the following website:http://www.freemap.jp/item/japan/japan1.html

Quantitative surveys in 2013

 In 2013 we used a 50-cm × 50-cm quadrat method for quantitative surveys of sessile organisms on the surface of tetrapods or other similar concrete structures. Results include the number of species, the number of individuals per square meter, and the wet-weight of whole organisms per square meter (Figs. 2–4, respectively).

 In terms of total numbers of sessile species in the intertidal zone, the species composition was dominated by the Mollusca and Arthropoda, followed by Annelida (Fig. 2). The maximum number of intertidal species was 25 at Hasaki Beach (Ibaraki Prefecture), followed by 22 at Urajiri (Fukushima Prefecture). The total number of species seemed to decrease with decreasing distance from FDNPP (regression analysis; P < 0.05 for sites south of FDNPP (n = 4) and P > 0.05 for those to the north (n = 3)), and the minimum of 8 species was at Okuma, in Fukushima Prefecture, located approximately 1 km south of FDNPP (Fig. 2). The similarity in species number between Tomioka fishing port, Fukushima Prefecture and Okuma, both of which are located south of FDNPP, was high and differed significantly from that between other sites (analysis of similarity (ANOSIM); P < 0.05, n = 7).

Figure 2. Total numbers of sessile species in intertidal zones, as sampled with a 50-cm × 50-cm quadrat in May–June 2013.
Purple star marks the location of Fukushima Daiichi Nuclear Power Plant (FDNPP). Dotted circle on map indicates a radius of 20 km from FDNPP.
*The partial map of Japan in this figure was modified by the authors from the map of Japan at the following website:
http://www.freemap.jp/item/japan/japan1.html

 Population densities, as indicated by the number of individuals per square meter, were higher in the lower and middle intertidal zones than in the upper intertidal zone. Mollusca (i.e., mussels such as Mytilus galloprovincialis and Septifer virgatus) and Arthropoda (i.e., barnacles such as Chthamalus challengeri) predominated at all sites surveyed (Fig. 3). There was a high level of similarity between the occurrences at Tomioka fishing port and Okuma (ANOSIM; P < 0.05, n = 7). Population densities of sessile organisms at Tomioka fishing port and Okuma were less than one-tenth to about one-fourth those at other sites (Hasaki Beach, Kujihama Beach, Urajiri and Ishinomaki). The population density of sessile organisms at Kubo-yaji, located approximately 1 km north of FDNPP, was comparable to those at Hasaki and Kujihama beaches, but approximately one-third those at Urajiri and Ishinomaki. Interestingly, however, the species composition of sessile organisms at Kubo-yaji differed markedly from that at other sites surveyed, in that the Arthropoda accounted for less than 1% of all sessile organisms collected (Fig. 3). Population densities of Arthropoda at sites around FDNPP (Tomioka fishing port, Okuma and Kubo-yaji) were lower than those at other sites (t-test; P = 0.050, n = 7).

Figure 3. Densities of sessile organisms (number/m2) in intertidal zones (by elevation). L: lower intertidal zone; M: middle intertidal zone; U: upper intertidal zone. Data were collected by using a 50-cm × 50-cm quadrat in May–June 2013.
Purple star marks the location of the Fukushima Daiichi Nuclear Power Plant (FDNPP).
Dotted circle indicates a 20-km radius from FDNPP. Pink dotted line represents the average number of individuals per square meter from surveys of sessile organisms conducted in May 1995 by using a quadrat method at 20 sites along the coast of Fukushima Prefecture 4. The average population density in 1995 was 7158 individuals/m2, consisting of Arthropoda (4593, 64.2%), Annelida (179, 2.5%), Mollusca (2348, 32.8%) and other organisms (38, 0.5%) 4.
*The partial map of Japan in this figure was modified by the authors from the map of Japan at the following website: http://www.freemap.jp/item/japan/japan1.html

 Maximum values for total wet-weight, defined as the combined wet-weight of whole organisms per square meter, were found in the lower intertidal zone at each site, followed by the middle and upper intertidal zones (Fig. 4). Mollusca predominated at all sites surveyed, followed by Arthropoda. Despite the similarity between Tomioka fishing port and Okuma, both located south of FDNPP (ANOSIM; P < 0.05, n = 7), the lower intertidal zone of Tomioka fishing port was quite different from all other zones (Fig. 4). The total wet-weights in each intertidal zone at Okuma were much lower than those at other sites. The total wet-weights in the middle and upper intertidal zones at Tomioka fishing port were also quite low and similar to those at Okuma. Although the total wet-weight per square meter in the lower intertidal zone at Tomioka fishing port was higher than that at Okuma, it was still only approximately one-half those at other sites.

Figure 4. Total wet-weight (g/m2) of sessile organisms in intertidal zones (by elevation). L: lower intertidal zone; M: middle intertidal zone; U: upper intertidal zone.
Data were collected by using a 50-cm × 50-cm quadrat in May–June 2013. Purple star marks the location of the Fukushima Daiichi Nuclear Power Plant (FDNPP). Dotted circle indicates a 20-km radius from FDNPP.
*The partial map of Japan in this figure was modified by the authors from the map of Japan at the following website: http://www.freemap.jp/item/japan/japan1.html

4. Perspectives

 In 2012, the number of species of intertidal biota declined significantly as the distance between the sampling sites and FDNPP became smaller (P < 0.001). No rock shell (Thais clavigera) specimens were collected at eight sites near FDNPP in Fukushima Prefecture in 2012. Because rock shell specimens were collected in 2012 at many sites in Miyagi and Iwate Prefectures, as well as at sites in northern Fukushima Prefecture, where the tsunami also hit, it is unlikely that the absence of rock shells around FDNPP was caused only by the tsunami. The absence of rock shells at sites close to FDNPP (from Hirono to Futaba Beach, a distance of about 30 km) also suggests that reproduction and recruitment did not occur there, or were less successful, in summer and autumn (the reproductive season and thereafter) in 2011.

 Our quantitative surveys in 2013 showed that the number of species and the population densities (i.e., the number of individuals and whole wet-weight of organisms per square meter) were significantly lower at sites south of FDNPP than at other sites (regression analysis; P < 0.05 (n = 4) for the number of species, ANOSIM; P < 0.05 (n = 7) for the number of species, P < 0.05 (n = 7) for the population densities). Population densities of Arthropoda (e.g., barnacles) were also lower at sites around FDNPP (i.e., Tomioka fishing port, Okuma and Kubo-yaji; P = 0.050, n = 7 (t-test)). These results all suggest that intertidal biota—especially Arthropoda—decreased in abundance around FDNPP after March 2011.

 TEPCO conducted similar seasonal surveys by using 30-cm × 30-cm quadrats at 20 sites in intertidal zones along the coast of Fukushima Prefecture in 1995, but only published a summary of their results 4. In May 1995, there was an average of 7158 individual sessile organisms per square meter, consisting of Arthropoda (4593, 64.2%), Annelida (179, 2.5%), Mollusca (2348, 32.8%) and other organisms (38, 0.5%) 4. It is therefore clear that Arthropoda predominated but that many other invertebrates were also present in Fukushima Prefecture in 1995, before the nuclear disaster in 2011. From this we conclude that the population densities and numbers of species of sessile organisms in the intertidal zones of Fukushima Prefecture have decreased since March 2011, especially south of FDNPP.

 It is evident that there were declines in the numbers of species and the population densities of intertidal biota, including Arthropoda and rock shells, at sites close to FDNPP (especially to the south) after the 2011 Great East Japan Earthquake. There are several possible causal factors. As already mentioned, it is unlikely that the tsunami was the only causal factor. If the tsunami was not the main cause of the declines near FDNPP, then other causes might include acute or sub-acute toxicities from harmful substances, or other factors associated with FDNPP. For example, the cooling water that leaked from the nuclear reactors directly to the sea between March and April 2011 is estimated to have included various radionuclides and several harmful chemicals 5,6 and therefore could have affected the nearby intertidal biota. More severe effects seem to have occurred along the coast south of FDNPP, and this may be due to the predominant local water currents.

 Further studies are therefore needed to clarify the main causal factors for declining intertidal biota around FDNPP, possibly through determining the acute or sub-acute toxicities of various radionuclides, chemicals or other factors, in laboratory experiments. Continued field observations of spatiotemporal changes in the populations of sessile organisms around FDNPP, including rock shell populations, are also necessary to ensure their recovery in the future. The focus should be on increasing population densities and reproductive success in terms of active behaviors such as mating and egg-laying and the subsequent successful recruitment of larvae and juveniles. It will also be necessary to conduct both field and laboratory studies to observe and evaluate possible multigenerational effects such as changes in reproductive success resulting from exposure to low-dose radiation and other environmental stressors.

5. References

1. Steinhauser, G., Brandl, A., & Johnson, T.E. Comparison of the Chernobyl and Fukushima nuclear accidents: A review of the environmental impacts. Sci. Total Environ. 470–471, 800–817 (2014).


2. Miyazawa, Y., Masumoto, Y., Varlamov, S.M., Miyama, T., Takigawa, M., Honda, M. & Saino, T. Inverse estimation of source parameters of oceanic radioactivity dispersion models associated with the Fukushima accident. Biogeosciences 10, 2349–2363 (2013).


3. Kanda, J. Deposition, discharge, spreading/dispersion and accumulation of radionuclides to the ocean in Contamination by radionuclides in the aquatic environment (ed. Kurokura, H.) 27–53 (Koseisha-Koseikaku, 2014). [in Japanese]


4. [TEPCO] Tokyo Electric Power Company. Marine organisms. in Environmental impact assessment, regarding the construction of Units 7 and 8 of the Fukushima Daiichi Nuclear Power Plant 5.11-1-5.11-14 (TEPCO, 2001). [in Japanese]


5. Nishihara, K., Iwamoto H. & Suyama K. Estimation of fuel compositions in Fukushima-Daiichi Nuclear Power Plant. JAEA-Data-Code-2012-018. (JAEA, 2012). [in Japanese]


6. Nuclear Regulation Authority, Japan, Summary for the interview to TEPCO (Tokyo Electric Power Company), regarding TEPCO’s methods for environmental monitoring. (2013) [in Japanese]. Available at: http://www.nsr.go.jp/data/000048877.pdf


6. Contct information

Toshihiro HORIGUCHI
Head, Ecosystem Impact Research Section
Center for Environmental Risk Research
National Institute for Environmental Studies
Tel: +81-29-850-2522 (direct)
E-mail: thorigu@nies.go.jp

7. Published article

Decline in intertidal biota after the 2011 Great East Japan Earthquake and Tsunami and the Fukushima nuclear disaster: field observations. Scientific Reports 6, 20416;
doi: 10.1038/srep20416 (2016).
URL: www.nature.com/articles/srep20416

8. Funding sources

This study was funded partly by the Ministry of the Environment, Government of Japan.